Advertisement

A focus on the role of platelets in liver regeneration: Do platelet-endothelial cell interactions initiate the regenerative process?

  • Jeremy Meyer
    Correspondence
    Corresponding author. Address: Division of Visceral and Transplantation Surgery, University Hospitals of Geneva, Rue Gabrielle-Perret-Gentil 4, 1211 Genève 14, Switzerland. Tel.: +41 76 316 19 84.
    Affiliations
    Division of Visceral and Transplantation Surgery, University Hospitals of Geneva, Rue Gabrielle-Perret-Gentil 4, 1211 Genève 14, Switzerland

    Unit of Surgical Research, University of Geneva, Rue Michel-Servet 1, 1206 Genève, Switzerland
    Search for articles by this author
  • Esma Lejmi
    Affiliations
    Unit of Surgical Research, University of Geneva, Rue Michel-Servet 1, 1206 Genève, Switzerland
    Search for articles by this author
  • Pierre Fontana
    Affiliations
    Division of Angiology and Haemostasis, University Hospitals of Geneva, Rue Gabrielle-Perret-Gentil 4, 1211 Genève 14, Switzerland

    Geneva Platelet Group, University of Geneva, Rue Michel-Servet 1, 1206 Genève, Switzerland
    Search for articles by this author
  • Philippe Morel
    Affiliations
    Division of Visceral and Transplantation Surgery, University Hospitals of Geneva, Rue Gabrielle-Perret-Gentil 4, 1211 Genève 14, Switzerland

    Unit of Surgical Research, University of Geneva, Rue Michel-Servet 1, 1206 Genève, Switzerland
    Search for articles by this author
  • Carmen Gonelle-Gispert
    Affiliations
    Unit of Surgical Research, University of Geneva, Rue Michel-Servet 1, 1206 Genève, Switzerland
    Search for articles by this author
  • Léo Bühler
    Affiliations
    Division of Visceral and Transplantation Surgery, University Hospitals of Geneva, Rue Gabrielle-Perret-Gentil 4, 1211 Genève 14, Switzerland

    Unit of Surgical Research, University of Geneva, Rue Michel-Servet 1, 1206 Genève, Switzerland
    Search for articles by this author

      Summary

      Platelets are involved in the early phases of liver regeneration. Moreover, platelet transfusion and thrombocytosis were recently shown to enhance hepatocyte proliferation. However, the precise mechanisms remain elusive. This review discusses the latest updates regarding the mechanisms by which platelets stimulate liver regeneration, focusing on their interactions with liver sinusoidal endothelial cells and on their fate within the liver.
      Following liver injury, platelets are recruited to and trapped within the liver, where they adhere to the endothelium. Subsequent platelet activation results in the release of platelet granules, which stimulate hepatocyte proliferation through activation of the Akt and ERK1/2 signalling pathways. Platelets activate liver sinusoidal endothelial cells, leading to the secretion of growth factors, such as interleukin-6. Finally, liver sinusoidal cells and hepatocytes can also internalize platelets, but the effects of this alternate process on liver regeneration remain to be explored. A better understanding of the mechanisms by which platelets stimulate liver regeneration could lead to improvement in post-operative organ function and allow hepatectomies of a greater extent to be performed.

      Keywords

      Abbreviations:

      PH (partial hepatectomy), LSEC (liver sinusoidal endothelial cell), TGF-β (transforming growth factor-β), IL-6 (interleukin-6), EGF (epidermal growth factor), HGF (hepatocyte growth factor), IGF-1 (insulin-like growth factor-1), LPS (lipopolysaccharide), VEGF (vascular endothelial growth factor), MAC-1 (macrophage-1 antigen)

      Linked Article

      • Reply to: “The role of platelets in liver regeneration – What don’t we know?”
        Journal of HepatologyVol. 63Issue 6
        • Preview
          We thank Dr Lisman and coworkers for their appreciation of our review article. This publication addressed the role of platelets in liver regeneration by summarizing current knowledge. A better understanding of how platelets act on liver regeneration could have a significant impact on therapies for life-threatening liver diseases. We proposed platelets to be recruited to the regenerating liver and to release molecules upon contact with liver sinusoidal endothelial cells (LSEC) that directly or indirectly act on hepatocyte proliferation [1].
        • Full-Text
        • PDF
      • Adverse effects of platelets on post-hepatectomy outcomes in patients with hepatocellular carcinoma
        Journal of HepatologyVol. 64Issue 2
        • Preview
          Recently, Meyer and colleagues [1] comprehensively reviewed the role of platelets in liver regeneration and its associated mechanisms. They illuminate that platelets can be recruited to the liver and then adhere to hepatic sinusoidal endothelial cells following liver injury. Subsequently, hepatocyte proliferation is stimulated by several molecules stored in platelets. Furthermore, techniques leading to elevated platelets, such as platelet transfusion, are proposed to accelerate liver regeneration, improve liver function, and reduce mortality among patients undergoing hepatectomy [1].
        • Full-Text
        • PDF
      • The role of platelets in liver regeneration – What don’t we know?
        Journal of HepatologyVol. 63Issue 6
        • Preview
          In an elegant review published in the Journal, Meyer and coworkers summarized current knowledge on the role of blood platelets in liver regeneration [1]. Better insight into how platelets act in amplifying liver regeneration following a partial hepatectomy might have important clinical consequences. Currently, no strategies to enhance liver regeneration to treat or avoid the ‘small for size syndrome’ are clinically available. Platelets are an unexpected, but interesting new target for clinical intervention aimed at accelerating liver regeneration.
        • Full-Text
        • PDF
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Hepatology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

      Author names in bold designate shared co-first authorship

        • Rendu F.
        • Brohard-Bohn B.
        The platelet release reaction: granules’ constituents, secretion and functions.
        Platelets. 2001; 12: 261-273
        • Nurden A.T.
        • Nurden P.
        • Sanchez M.
        • Andia I.
        • Anitua E.
        Platelets and wound healing.
        Front Biosci. 2008; 13: 3532-3548
        • Semple J.W.
        • Italiano Jr., J.E.
        • Freedman J.
        Platelets and the immune continuum.
        Nat Rev Immunol. 2011; 11: 264-274
        • Coppinger J.A.
        • Maguire P.B.
        Insights into the platelet releasate.
        Curr Pharm Des. 2007; 13: 2640-2646
        • Tomikawa M.
        • Hashizume M.
        • Highashi H.
        • Ohta M.
        • Sugimachi K.
        The role of the spleen, platelets, and plasma hepatocyte growth factor activity on hepatic regeneration in rats.
        J Am Coll Surg. 1996; 182: 12-16
        • Murata S.
        • Hashimoto I.
        • Nakano Y.
        • Myronovych A.
        • Watanabe M.
        • Ohkohchi N.
        Single administration of thrombopoietin prevents progression of liver fibrosis and promotes liver regeneration after partial hepatectomy in cirrhotic rats.
        Ann Surg. 2008; 248: 821-828
        • Murata S.
        • Ohkohchi N.
        • Matsuo R.
        • Ikeda O.
        • Myronovych A.
        • Hoshi R.
        Platelets promote liver regeneration in early period after hepatectomy in mice.
        World J Surg. 2007; 31: 808-816
        • Myronovych A.
        • Murata S.
        • Chiba M.
        • Matsuo R.
        • Ikeda O.
        • Watanabe M.
        • et al.
        Role of platelets on liver regeneration after 90% hepatectomy in mice.
        J Hepatol. 2008; 49: 363-372
        • Shimabukuro R.
        • Kawanaka H.
        • Tomikawa M.
        • Akahoshi T.
        • Konishi K.
        • Yoshida D.
        • et al.
        Effect of thrombopoietin on platelet counts and liver regeneration after partial hepatectomy in a rat model.
        Surg Today. 2009; 39: 1054-1059
        • Matsuo R.
        • Nakano Y.
        • Ohkohchi N.
        Platelet administration via the portal vein promotes liver regeneration in rats after 70% hepatectomy.
        Ann Surg. 2011; 253: 759-763
        • Lesurtel M.
        • Graf R.
        • Aleil B.
        • Walther D.J.
        • Tian Y.
        • Jochum W.
        • et al.
        Platelet-derived serotonin mediates liver regeneration.
        Science. 2006; 312: 104-107
        • Michalopoulos G.K.
        Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas.
        Am J Pathol. 2010; 176: 2-13
        • Taub R.
        Liver regeneration: from myth to mechanism.
        Nat Rev Mol Cell Biol. 2004; 5: 836-847
        • Brown T.L.
        • Patil S.
        • Howe P.H.
        Analysis of TGF-beta-inducible apoptosis.
        Methods Mol Biol. 2000; 142: 149-167
        • Bursch W.
        • Oberhammer F.
        • Jirtle R.L.
        • Askari M.
        • Sedivy R.
        • Grasl-Kraupp B.
        • et al.
        Transforming growth factor-beta 1 as a signal for induction of cell death by apoptosis.
        Br J Cancer. 1993; 67: 531-536
        • Si X.H.
        • Yang L.J.
        Extraction and purification of TGFbeta and its effect on the induction of apoptosis of hepatocytes.
        World J Gastroenterol. 2001; 7: 527-531
        • Hong F.
        • Nguyen V.A.
        • Shen X.
        • Kunos G.
        • Gao B.
        Rapid activation of protein kinase B/Akt has a key role in antiapoptotic signaling during liver regeneration.
        Biochem Biophys Res Commun. 2000; 279: 974-979
        • Matsuo R.
        • Ohkohchi N.
        • Murata S.
        • Ikeda O.
        • Nakano Y.
        • Watanabe M.
        • et al.
        Platelets strongly induce hepatocyte proliferation with IGF-1 and HGF in vitro.
        J Surg Res. 2008; 145: 279-286
        • Murata S.
        • Matsuo R.
        • Ikeda O.
        • Myronovych A.
        • Watanabe M.
        • Hisakura K.
        • et al.
        Platelets promote liver regeneration under conditions of Kupffer cell depletion after hepatectomy in mice.
        World J Surg. 2008; 32: 1088-1096
        • Endo Y.
        • Nakamura M.
        The effect of lipopolysaccharide, interleukin-1 and tumour necrosis factor on the hepatic accumulation of 5-hydroxytryptamine and platelets in the mouse.
        Br J Pharmacol. 1992; 105: 613-619
        • Jonnakuty C.
        • Gragnoli C.
        What do we know about serotonin?.
        J Cell Physiol. 2008; 217: 301-306
        • Nakamura M.
        • Shibazaki M.
        • Nitta Y.
        • Endo Y.
        Translocation of platelets into Disse spaces and their entry into hepatocytes in response to lipopolysaccharides, interleukin-1 and tumour necrosis factor: the role of Kupffer cells.
        J Hepatol. 1998; 28: 991-999
        • Helmy A.
        • Kishta S.
        • Khaled E.
        Interrelation between peripheral platelet count and platelet activation during and after liver surgery in pigs.
        Blood Coagul Fibrinolysis. 2010; 21: 237-241
        • Wack K.E.
        • Ross M.A.
        • Zegarra V.
        • Sysko L.R.
        • Watkins S.C.
        • Stolz D.B.
        Sinusoidal ultrastructure evaluated during the revascularization of regenerating rat liver.
        Hepatology. 2001; 33: 363-378
        • Cornell R.P.
        Gut-derived endotoxin elicits hepatotrophic factor secretion for liver regeneration.
        Am J Physiol. 1985; 249: R551-562
        • Cornell R.P.
        Restriction of gut-derived endotoxin impairs DNA synthesis for liver regeneration.
        Am J Physiol. 1985; 249: R563-569
        • Zhang J.N.
        • Bergeron A.L.
        • Yu Q.
        • Sun C.
        • McIntire L.V.
        • Lopez J.A.
        • et al.
        Platelet aggregation and activation under complex patterns of shear stress.
        Thromb Haemost. 2002; 88: 817-821
        • Marubashi S.
        • Sakon M.
        • Nagano H.
        • Gotoh K.
        • Hashimoto K.
        • Kubota M.
        • et al.
        Effect of portal hemodynamics on liver regeneration studied in a novel portohepatic shunt rat model.
        Surgery. 2004; 136: 1028-1037
        • Lee S.
        • Broelsch C.E.
        • Flamant Y.M.
        • Chandler J.G.
        • Charters 3rd, A.C.
        • Orloff M.J.
        Liver regeneration after portacaval transportation in rats.
        Surgery. 1975; 77: 144-149
        • Wisse E.
        An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids.
        J Ultrastruct Res. 1970; 31: 125-150
        • Maher J.J.
        Cell-specific expression of hepatocyte growth factor in liver. Upregulation in sinusoidal endothelial cells after carbon tetrachloride.
        J Clin Investig. 1993; 91: 2244-2252
        • Ding B.S.
        • Nolan D.J.
        • Butler J.M.
        • James D.
        • Babazadeh A.O.
        • Rosenwaks Z.
        • et al.
        Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration.
        Nature. 2010; 468: 310-315
        • LeCouter J.
        • Moritz D.R.
        • Li B.
        • Phillips G.L.
        • Liang X.H.
        • Gerber H.P.
        • et al.
        Angiogenesis-independent endothelial protection of liver: role of VEGFR-1.
        Science. 2003; 299: 890-893
        • Ping C.
        • Xiaoling D.
        • Jin Z.
        • Jiahong D.
        • Jiming D.
        • Lin Z.
        Hepatic sinusoidal endothelial cells promote hepatocyte proliferation early after partial hepatectomy in rats.
        Arch Med Res. 2006; 37: 576-583
        • Hu J.
        • Srivastava K.
        • Wieland M.
        • Runge A.
        • Mogler C.
        • Besemfelder E.
        • et al.
        Endothelial cell-derived angiopoietin-2 controls liver regeneration as a spatiotemporal rheostat.
        Science. 2014; 343: 416-419
        • Sindram D.
        • Porte R.J.
        • Hoffman M.R.
        • Bentley R.C.
        • Clavien P.A.
        Platelets induce sinusoidal endothelial cell apoptosis upon reperfusion of the cold ischemic rat liver.
        Gastroenterology. 2000; 118: 183-191
        • Lentsch A.B.
        • Kato A.
        • Yoshidome H.
        • McMasters K.M.
        • Edwards M.J.
        Inflammatory mechanisms and therapeutic strategies for warm hepatic ischemia/reperfusion injury.
        Hepatology. 2000; 32: 169-173
        • Massberg S.
        • Enders G.
        • Leiderer R.
        • Eisenmenger S.
        • Vestweber D.
        • Krombach F.
        • et al.
        Platelet-endothelial cell interactions during ischemia/reperfusion: the role of P-selectin.
        Blood. 1998; 92: 507-515
        • Tsujikawa A.
        • Kiryu J.
        • Nonaka A.
        • Yamashiro K.
        • Nishiwaki H.
        • Tojo S.J.
        • et al.
        In vivo evaluation of platelet–endothelial interactions in retinal microcirculation of rats.
        Invest Ophthalmol Vis Sci. 1999; 40: 2918-2924
        • Gotsch U.
        • Jager U.
        • Dominis M.
        • Vestweber D.
        Expression of P-selectin on endothelial cells is upregulated by LPS and TNF-alpha in vivo.
        Cell Adhes Commun. 1994; 2: 7-14
        • Zhang G.
        • Han J.
        • Welch E.J.
        • Ye R.D.
        • Voyno-Yasenetskaya T.A.
        • Malik A.B.
        • et al.
        Lipopolysaccharide stimulates platelet secretion and potentiates platelet aggregation via TLR4/MyD88 and the cGMP-dependent protein kinase pathway.
        J Immunol. 2009; 182: 7997-8004
        • Andonegui G.
        • Kerfoot S.M.
        • McNagny K.
        • Ebbert K.V.
        • Patel K.D.
        • Kubes P.
        Platelets express functional Toll-like receptor-4.
        Blood. 2005; 106: 2417-2423
        • Ward J.R.
        • Bingle L.
        • Judge H.M.
        • Brown S.B.
        • Storey R.F.
        • Whyte M.K.
        • et al.
        Agonists of toll-like receptor (TLR)2 and TLR4 are unable to modulate platelet activation by adenosine diphosphate and platelet activating factor.
        Thromb Haemost. 2005; 94: 831-838
        • Jenne C.N.
        • Wong C.H.
        • Petri B.
        • Kubes P.
        The use of spinning-disk confocal microscopy for the intravital analysis of platelet dynamics in response to systemic and local inflammation.
        PLoS One. 2011; 6: e25109
        • McDonald B.
        • Urrutia R.
        • Yipp B.G.
        • Jenne C.N.
        • Kubes P.
        Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis.
        Cell Host Microbe. 2012; 12: 324-333
        • Russell J.
        • Cooper D.
        • Tailor A.
        • Stokes K.Y.
        • Granger D.N.
        Low venular shear rates promote leukocyte-dependent recruitment of adherent platelets.
        Am J Physiol Gastrointest Liver Physiol. 2003; 284: G123-129
        • Lesurtel M.
        • Clavien P.A.
        Platelet-derived serotonin: translational implications for liver regeneration.
        Hepatology. 2014; 60: 30-33
        • Starlinger P.
        • Assinger A.
        • Haegele S.
        • Wanek D.
        • Zikeli S.
        • Schauer D.
        • et al.
        Evidence for serotonin as a relevant inducer of liver regeneration after liver resection in humans.
        Hepatology. 2014; 60: 257-266
        • Alkozai E.M.
        • van Faassen M.
        • Kema I.P.
        • Porte R.J.
        • Lisman T.
        Evidence against a role of serotonin in liver regeneration in humans.
        Hepatology. 2014;
        • Walther D.J.
        • Peter J.U.
        • Winter S.
        • Holtje M.
        • Paulmann N.
        • Grohmann M.
        • et al.
        Serotonylation of small GTPases is a signal transduction pathway that triggers platelet alpha-granule release.
        Cell. 2003; 115: 851-862
        • Assoian R.K.
        • Komoriya A.
        • Meyers C.A.
        • Miller D.M.
        • Sporn M.B.
        Transforming growth factor-beta in human platelets. Identification of a major storage site, purification, and characterization.
        J Biol Chem. 1983; 258: 7155-7160
        • Ma L.
        • Perini R.
        • McKnight W.
        • Dicay M.
        • Klein A.
        • Hollenberg M.D.
        • et al.
        Proteinase-activated receptors 1 and 4 counter-regulate endostatin and VEGF release from human platelets.
        Proc Natl Acad Sci USA. 2005; 102: 216-220
        • Italiano Jr., J.E.
        • Richardson J.L.
        • Patel-Hett S.
        • Battinelli E.
        • Zaslavsky A.
        • Short S.
        • et al.
        Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released.
        Blood. 2008; 111: 1227-1233
        • Klement G.L.
        • Yip T.T.
        • Cassiola F.
        • Kikuchi L.
        • Cervi D.
        • Podust V.
        • et al.
        Platelets actively sequester angiogenesis regulators.
        Blood. 2009; 113: 2835-2842
        • Greene A.K.
        • Wiener S.
        • Puder M.
        • Yoshida A.
        • Shi B.
        • Perez-Atayde A.R.
        • et al.
        Endothelial-directed hepatic regeneration after partial hepatectomy.
        Ann Surg. 2003; 237: 530-535
        • Robson S.C.
        • Sevigny J.
        • Zimmermann H.
        The E-NTPDase family of ectonucleotidases: Structure function relationships and pathophysiological significance.
        Purinergic Signalling. 2006; 2: 409-430
        • Beldi G.
        • Wu Y.
        • Sun X.
        • Imai M.
        • Enjyoji K.
        • Csizmadia E.
        • et al.
        Regulated catalysis of extracellular nucleotides by vascular CD39/ENTPD1 is required for liver regeneration.
        Gastroenterology. 2008; 135: 1751-1760
        • Crumm S.
        • Cofan M.
        • Juskeviciute E.
        • Hoek J.B.
        Adenine nucleotide changes in the remnant liver: An early signal for regeneration after partial hepatectomy.
        Hepatology. 2008; 48: 898-908
        • Atkinson B.
        • Dwyer K.
        • Enjyoji K.
        • Robson S.C.
        Ecto-nucleotidases of the CD39/NTPDase family modulate platelet activation and thrombus formation: Potential as therapeutic targets.
        Blood Cells Mol Dis. 2006; 36: 217-222
        • Enjyoji K.
        • Sevigny J.
        • Lin Y.
        • Frenette P.S.
        • Christie P.D.
        • Esch 2nd, J.S.
        • et al.
        Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation.
        Nat Med. 1999; 5: 1010-1017
        • Coppinger J.A.
        • Cagney G.
        • Toomey S.
        • Kislinger T.
        • Belton O.
        • McRedmond J.P.
        • et al.
        Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions.
        Blood. 2004; 103: 2096-2104
        • Kawasaki T.
        • Murata S.
        • Takahashi K.
        • Nozaki R.
        • Ohshiro Y.
        • Ikeda N.
        • et al.
        Activation of human liver sinusoidal endothelial cell by human platelets induces hepatocyte proliferation.
        J Hepatol. 2010; 53: 648-654
        • Nowatari T.
        • Murata S.
        • Nakayama K.
        • Sano N.
        • Maruyama T.
        • Nozaki R.
        • et al.
        Sphingosine 1-phosphate has anti-apoptotic effect on liver sinusoidal endothelial cells and proliferative effect on hepatocytes in a paracrine manner in human.
        Hepatol Res. 2014;
        • Yatomi Y.
        • Ohmori T.
        • Rile G.
        • Kazama F.
        • Okamoto H.
        • Sano T.
        • et al.
        Sphingosine 1-phosphate as a major bioactive lysophospholipid that is released from platelets and interacts with endothelial cells.
        Blood. 2000; 96: 3431-3438
        • Nomura S.
        • Tandon N.N.
        • Nakamura T.
        • Cone J.
        • Fukuhara S.
        • Kambayashi J.
        High-shear-stress-induced activation of platelets and microparticles enhances expression of cell adhesion molecules in THP-1 and endothelial cells.
        Atherosclerosis. 2001; 158: 277-287
        • Wisse E.
        An ultrastructural characterization of the endothelial cell in the rat liver sinusoid under normal and various experimental conditions, as a contribution to the distinction between endothelial and Kupffer cells.
        J Ultrastruct Res. 1972; 38: 528-562
        • Elvevold K.
        • Smedsrod B.
        • Martinez I.
        The liver sinusoidal endothelial cell: a cell type of controversial and confusing identity.
        Am J Physiol Gastrointest Liver Physiol. 2008; 294: G391-400
        • Smedsrod B.
        • Le Couteur D.
        • Ikejima K.
        • Jaeschke H.
        • Kawada N.
        • Naito M.
        • et al.
        Hepatic sinusoidal cells in health and disease: update from the 14th International Symposium.
        Liver Int. 2009; 29: 490-501
        • Smedsrod B.
        • Pertoft H.
        • Gustafson S.
        • Laurent T.C.
        Scavenger functions of the liver endothelial cell.
        Biochem J. 1990; 266: 313-327
        • Ekser B.
        • Long C.
        • Echeverri G.J.
        • Hara H.
        • Ezzelarab M.
        • Lin C.C.
        • et al.
        Impact of thrombocytopenia on survival of baboons with genetically modified pig liver transplants: clinical relevance.
        Am J Transplant. 2010; 10: 273-285
        • Tector A.J.
        • Fridell J.A.
        • Elias N.
        • Watanabe T.
        • Salazar J.
        • Greinke D.
        • et al.
        Aberrations in hemostasis and coagulation in untreated discordant hepatic xenotransplantation: studies in the dog-to-pig model.
        Liver Transplant. 2002; 8: 153-159
        • Burlak C.
        • Paris L.L.
        • Chihara R.K.
        • Sidner R.A.
        • Reyes L.M.
        • Downey S.M.
        • et al.
        The fate of human platelets perfused through the pig liver: implications for xenotransplantation.
        Xenotransplantation. 2010; 17: 350-361
        • Hickman R.
        • Parker J.R.
        • Saunders S.J.
        • Terblanche J.
        Platelet adherence in the pig liver perfused with human blood.
        Transplantation. 1972; 13: 195-198
        • Paris L.L.
        • Chihara R.K.
        • Sidner R.A.
        • Tector A.J.
        • Burlak C.
        Differences in human and porcine platelet oligosaccharides may influence phagocytosis by liver sinusoidal cells in vitro.
        Xenotransplantation. 2012; 19: 31-39
        • Chihara R.K.
        • Paris L.L.
        • Reyes L.M.
        • Sidner R.A.
        • Estrada J.L.
        • Downey S.M.
        • et al.
        Primary porcine Kupffer cell phagocytosis of human platelets involves the CD18 receptor.
        Transplantation. 2011; 92: 739-744
        • Paris L.L.
        • Chihara R.K.
        • Reyes L.M.
        • Sidner R.A.
        • Estrada J.L.
        • Downey S.M.
        • et al.
        ASGR1 expressed by porcine enriched liver sinusoidal endothelial cells mediates human platelet phagocytosis in vitro.
        Xenotransplantation. 2011; 18: 245-251
        • Wang Z.Y.
        • Paris L.L.
        • Chihara R.K.
        • Tector A.J.
        • Burlak C.
        Immortalized porcine liver sinusoidal endothelial cells: an in vitro model of xenotransplantation-induced thrombocytopenia.
        Xenotransplantation. 2012; 19: 249-255
        • Peng Q.
        • Yeh H.
        • Wei L.
        • Enjyoj K.
        • Machaidze Z.
        • Csizmad E.
        • et al.
        Mechanisms of xenogeneic baboon platelet aggregation and phagocytosis by porcine liver sinusoidal endothelial cells.
        PLoS One. 2012; 7: e47273
        • Sorensen A.L.
        • Rumjantseva V.
        • Nayeb-Hashemi S.
        • Clausen H.
        • Hartwig J.H.
        • Wandall H.H.
        • et al.
        Role of sialic acid for platelet life span: exposure of beta-galactose results in the rapid clearance of platelets from the circulation by asialoglycoprotein receptor-expressing liver macrophages and hepatocytes.
        Blood. 2009; 114: 1645-1654
        • Rumjantseva V.
        • Hoffmeister K.M.
        Novel and unexpected clearance mechanisms for cold platelets.
        Transfus Apher Sci. 2010; 42: 63-70
        • Kolb-Bachofen V.
        • Schlepper-Schafer J.
        • Vogell W.
        • Kolb H.
        Electron microscopic evidence for an asialoglycoprotein receptor on Kupffer cells: localization of lectin-mediated endocytosis.
        Cell. 1982; 29: 859-866
        • Weigel P.H.
        Characterization of the asialoglycoprotein receptor on isolated rat hepatocytes.
        J Biol Chem. 1980; 255: 6111-6120
        • Hoffmeister K.M.
        • Felbinger T.W.
        • Falet H.
        • Denis C.V.
        • Bergmeier W.
        • Mayadas T.N.
        • et al.
        The clearance mechanism of chilled blood platelets.
        Cell. 2003; 112: 87-97
        • Markovic N.
        • McCaig L.A.
        • Stephen J.
        • Mizuguchi S.
        • Veldhuizen R.A.
        • Lewis J.F.
        • et al.
        Mediators released from LPS-challenged lungs induce inflammatory responses in liver vascular endothelial cells and neutrophilic leukocytes.
        Am J Physiol Gastrointest Liver Physiol. 2009; 297: G1066-1076
        • Kuckleburg C.J.
        • Tiwari R.
        • Czuprynski C.J.
        Endothelial cell apoptosis induced by bacteria-activated platelets requires caspase-8 and -9 and generation of reactive oxygen species.
        Thromb Haemost. 2008; 99: 363-372
        • Jiang P.
        • Ren Y.L.
        • Lan Y.
        • Li J.L.
        • Luo J.
        • Li J.
        • et al.
        Phagocytosis of platelets enhances endothelial cell survival under serum deprivation.
        Exp Biol Med. 2015;
        • Kauffmann R.
        • Fong Y.
        Post-hepatectomy liver failure.
        Hepatobiliary Surg Nutr. 2014; 3: 238-246
        • Shoup M.
        • Gonen M.
        • D’Angelica M.
        • Jarnagin W.R.
        • DeMatteo R.P.
        • Schwartz L.H.
        • et al.
        Volumetric analysis predicts hepatic dysfunction in patients undergoing major liver resection.
        J Gastrointest Surg. 2003; 7: 325-330
        • Farges O.
        • Belghiti J.
        • Kianmanesh R.
        • Regimbeau J.M.
        • Santoro R.
        • Vilgrain V.
        • et al.
        Portal vein embolization before right hepatectomy: prospective clinical trial.
        Ann Surg. 2003; 237: 208-217
        • Kaneko K.
        • Shirai Y.
        • Wakai T.
        • Yokoyama N.
        • Akazawa K.
        • Hatakeyama K.
        Low preoperative platelet counts predict a high mortality after partial hepatectomy in patients with hepatocellular carcinoma.
        World J Gastroenterol. 2005; 11: 5888-5892
        • Poon R.T.
        • Fan S.T.
        • Lo C.M.
        • Liu C.L.
        • Lam C.M.
        • Yuen W.K.
        • et al.
        Improving perioperative outcome expands the role of hepatectomy in management of benign and malignant hepatobiliary diseases: analysis of 1222 consecutive patients from a prospective database.
        Ann Surg. 2004; 240 ([discussion 708–610]): 698-708
        • Taketomi A.
        • Kitagawa D.
        • Itoh S.
        • Harimoto N.
        • Yamashita Y.
        • Gion T.
        • et al.
        Trends in morbidity and mortality after hepatic resection for hepatocellular carcinoma: an institute’s experience with 625 patients.
        J Am Coll Surg. 2007; 204: 580-587
        • Alkozai E.M.
        • Nijsten M.W.
        • de Jong K.P.
        • de Boer M.T.
        • Peeters P.M.
        • Slooff M.J.
        • et al.
        Immediate postoperative low platelet count is associated with delayed liver function recovery after partial liver resection.
        Ann Surg. 2010; 251: 300-306
        • Boleslawski E.
        • Petrovai G.
        • Truant S.
        • Dharancy S.
        • Duhamel A.
        • Salleron J.
        • et al.
        Hepatic venous pressure gradient in the assessment of portal hypertension before liver resection in patients with cirrhosis.
        Br J Surg. 2012; 99: 855-863
        • Kim J.
        • Yi N.J.
        • Shin W.Y.
        • Kim T.
        • Lee K.U.
        • Suh K.S.
        Platelet transfusion can be related to liver regeneration after living donor liver transplantation.
        World J Surg. 2010; 34: 1052-1058
        • Marubashi S.
        • Dono K.
        • Miyamoto A.
        • Takeda Y.
        • Nagano H.
        • Umeshita K.
        • et al.
        Impact of graft size on postoperative thrombocytopenia in living donor liver transplant.
        Arch Surg. 2007; 142: 1054-1058
        • Cescon M.
        • Sugawara Y.
        • Takayama T.
        • Seyama Y.
        • Sano K.
        • Imamura H.
        • et al.
        Role of splenectomy in living-donor liver transplantation for adults.
        Hepatogastroenterology. 2002; 49: 721-723
        • Chatterjee M.
        • Huang Z.
        • Zhang W.
        • Jiang L.
        • Hultenby K.
        • Zhu L.
        • et al.
        Distinct platelet packaging, release, and surface expression of proangiogenic and antiangiogenic factors on different platelet stimuli.
        Blood. 2011; 117: 3907-3911
        • Kiefel V.
        Reactions induced by platelet transfusions.
        Transfus Med Hemother. 2008; 35: 354-358
        • Di Sabatino A.
        • Carsetti R.
        • Corazza G.R.
        Post-splenectomy and hyposplenic states.
        Lancet. 2011; 378: 86-97
        • Geraud C.
        • Schledzewski K.
        • Demory A.
        • Klein D.
        • Kaus M.
        • Peyre F.
        • et al.
        Liver sinusoidal endothelium: a microenvironment-dependent differentiation program in rat including the novel junctional protein liver endothelial differentiation-associated protein-1.
        Hepatology. 2010; 52: 313-326
        • Taniguchi E.
        • Sakisaka S.
        • Matsuo K.
        • Tanikawa K.
        • Sata M.
        Expression and role of vascular endothelial growth factor in liver regeneration after partial hepatectomy in rats.
        J Histochem Cytochem. 2001; 49: 121-130