Rejuvenation: an integrated approach to regenerative medicine

Sykova E, Homola A, Mazanec R, Lachmann H, Konradova SL, Kobylka P, Padr R, Neuwirth J, Komrska V, Vavra V, et al.: Autologous bone marrow transplantation in patients with subacute and chronic spinal cord injury. Cell Transplant 2006, 15: 675–687.

Geffner LF, Santacruz P, Izurieta M, Flor L, Maldonado B, Auad AH, Montenegro X, Gonzalez R, Silva F: Administration of autologous bone marrow stem cells into spinal cord injury patients via multiple routes is safe and improves their quality of life: comprehensive case studies. Cell Transplant 2008, 17: 1277–1293.

Horwitz EM, Gordon PL, Koo WK, Marx JC, Neel MD, McNall RY, Muul L, Hofmann T: Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci U S A 2002, 99: 8932–8937.

De Coppi P: Regenerative medicine for congenital malformations. J Pediatr Surg 2013, 48: 273–280.

Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB: Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 2006, 367: 1241–1246.

Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Holschermann H, Yu J, Corti R, Mathey DG, Hamm CW, et al.: Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 2006, 355: 1210–1221.

Binder S, Stanzel BV, Krebs I, Glittenberg C: Transplantation of the RPE in AMD. Prog Retin Eye Res 2007, 26: 516–554.

Yaniz-Galende E, Chen J, Chemaly E, Liang L, Hulot JS, McCollum L, Arias T, Fuster V, Zsebo KM, Hajjar RJ: Stem cell factor gene transfer promotes cardiac repair after myocardial infarction via in situ recruitment and expansion of c-kit+ cells. Circ Res 2012, 111: 1434–1445.

Christie JD, Edwards LB, Kucheryavaya AY, Benden C, Dipchand AI, Dobbels F, Kirk R, Rahmel AO, Stehlik J, Hertz MI: The registry of the international society for heart and lung transplantation: 29th adult lung and heart-lung transplant report-2012. J Heart Lung Transplant 2012, 31: 1073–1086.

Bainbridge JW, Smith AJ, Barker SS, Robbie S, Henderson R, Balaggan K, Viswanathan A, Holder GE, Stockman A, Tyler N, et al.: Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 2008, 358: 2231–2239.

Hatzistergos KE, Quevedo H, Oskouei BN, Hu Q, Feigenbaum GS, Margitich IS, Mazhari R, Boyle AJ, Zambrano JP, Rodriguez JE, et al.: Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res 2010, 107: 913–922.

Oberpenning F, Meng J, Yoo JJ, Atala A: De novo reconstitution of a functional mammalian urinary bladder by tissue engineering. Nat Biotechnol 1999, 17: 149–155.

Poss KD, Wilson LG, Keating MT: Heart regeneration in zebrafish. Science 2002, 298: 2188–2190.

Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN, Sadek HA: Transient regenerative potential of the neonatal mouse heart. Science 2011, 331: 1078–1080.

Kajstura J, Rota M, Cappetta D, Ogorek B, Arranto C, Bai Y, Ferreira-Martins J, Signore S, Sanada F, Matsuda A, et al.: Cardiomyogenesis in the aging and failing human heart. Circulation 2012, 126: 1869–1881.

Garrett WE Jr, Seaber AV, Boswick J, Urbaniak JR, Goldner JL: Recovery of skeletal muscle after laceration and repair. J Hand Surg [Am] 1984, 9: 683–692.

Haubner BJ, Adamowicz-Brice M, Khadayate S, Tiefenthaler V, Metzler B, Aitman T, Penninger JM: Complete cardiac regeneration in a mouse model of myocardial infarction. Aging (Albany NY) 2012, 4: 966–977.

Nirula R, Gentilello LM: Futility of resuscitation criteria for the "young" old and the "old" old trauma patient: a national trauma data bank analysis. J Trauma 2004, 57: 37–41.

Kuhne CA, Ruchholtz S, Kaiser GM, Nast-Kolb D: Mortality in severely injured elderly trauma patients–when does age become a risk factor? World J Surg 2005, 29: 1476–1482.

Sadeh M: Effects of aging on skeletal muscle regeneration. J Neurol Sci 1988, 87: 67–74.

Conboy IM, Conboy MJ, Smythe GM, Rando TA: Notch-mediated restoration of regenerative potential to aged muscle. Science 2003, 302: 1575–1577.

Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA: Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 2001, 107: 1395–1402.

Laflamme MA, Myerson D, Saffitz JE, Murry CE: Evidence for cardiomyocyte repopulation by extracardiac progenitors in transplanted human hearts. Circ Res 2002, 90: 634–640.

Paoni NF, Peale F, Wang F, Errett-Baroncini C, Steinmetz H, Toy K, Bai W, Williams PM, Bunting S, Gerritsen ME, Powell-Braxton L: Time course of skeletal muscle repair and gene expression following acute hind limb ischemia in mice. Physiol Genomics 2002, 11: 263–272.

Bosch-Marce M, Okuyama H, Wesley JB, Sarkar K, Kimura H, Liu YV, Zhang H, Strazza M, Rey S, Savino L, et al.: Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia. Circ Res 2007, 101: 1310–1318.

Cai Z, Zhong H, Bosch-Marce M, Fox-Talbot K, Wang L, Wei C, Trush MA, Semenza GL: Complete loss of ischaemic preconditioning-induced cardioprotection in mice with partial deficiency of HIF-1 alpha. Cardiovasc Res 2008, 77: 463–470.

Vandervelde S, van Luyn MJ, Rozenbaum MH, Petersen AH, Tio RA, Harmsen MC: Stem cell-related cardiac gene expression early after murine myocardial infarction. Cardiovasc Res 2007, 73: 783–793.

Kucia M, Dawn B, Hunt G, Guo Y, Wysoczynski M, Majka M, Ratajczak J, Rezzoug F, Ildstad ST, Bolli R, Ratajczak MZ: Cells expressing early cardiac markers reside in the bone marrow and are mobilized into the peripheral blood after myocardial infarction. Circ Res 2004, 95: 1191–1199.

Kim CH, Cho YS, Chun YS, Park JW, Kim MS: Early expression of myocardial HIF-1alpha in response to mechanical stresses: regulation by stretch-activated channels and the phosphatidylinositol 3-kinase signaling pathway. Circ Res 2002, 90: E25-E33.

Prior BM, Lloyd PG, Ren J, Li H, Yang HT, Laughlin MH, Terjung RL: Time course of changes in collateral blood flow and isolated vessel size and gene expression after femoral artery occlusion in rats. Am J Physiol Heart Circ Physiol 2004, 287: H2434-H2447.

Chevion M, Jiang Y, Har-El R, Berenshtein E, Uretzky G, Kitrossky N: Copper and iron are mobilized following myocardial ischemia: possible predictive criteria for tissue injury. Proc Natl Acad Sci U S A 1993, 90: 1102–1106.

Feng W, Ye F, Xue W, Zhou Z, Kang YJ: Copper regulation of hypoxia-inducible factor-1 activity. Mol Pharmacol 2009, 75: 174–182.

Jiang Y, Reynolds C, Xiao C, Feng W, Zhou Z, Rodriguez W, Tyagi SC, Eaton JW, Saari JT, Kang YJ: Dietary copper supplementation reverses hypertrophic cardiomyopathy induced by chronic pressure overload in mice. J Exp Med 2007, 204: 657–666.

Date T, Mochizuki S, Belanger AJ, Yamakawa M, Luo Z, Vincent KA, Cheng SH, Gregory RJ, Jiang C: Expression of constitutively stable hybrid hypoxia-inducible factor-1alpha protects cultured rat cardiomyocytes against simulated ischemia-reperfusion injury. Am J Physiol Cell Physiol 2005, 288: C314-C320.

Natarajan R, Salloum FN, Fisher BJ, Kukreja RC, Fowler AA 3rd: Hypoxia inducible factor-1 activation by prolyl 4-hydroxylase-2 gene silencing attenuates myocardial ischemia reperfusion injury. Circ Res 2006, 98: 133–140.

DeWood MA, Spores J, Notske R, Mouser LT, Burroughs R, Golden MS, Lang HT: Prevalence of total coronary occlusion during the early hours of transmural myocardial infarction. N Engl J Med 1980, 303: 897–902.

Fishbein MC, Maclean D, Maroko PR: Experimental myocardial infarction in the rat: qualitative and quantitative changes during pathologic evolution. Am J Pathol 1978, 90: 57–70.

Kamba T, Tam BY, Hashizume H, Haskell A, Sennino B, Mancuso MR, Norberg SM, O'Brien SM, Davis RB, Gowen LC, et al.: VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature. Am J Physiol Heart Circ Physiol 2006, 290: H560-H576.

Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Siebels M, Negrier S, Chevreau C, Solska E, Desai AA, et al.: Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007, 356: 125–134.

Gordon MS, Cunningham D: Managing patients treated with bevacizumab combination therapy. Oncology 2005,69(Suppl 3):25–33.

Senyo SE, Steinhauser ML, Pizzimenti CL, Yang VK, Cai L, Wang M, Wu TD, Guerquin-Kern JL, Lechene CP, Lee RT: Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013, 493: 433–436.

Jopling C, Sleep E, Raya M, Marti M, Raya A, Izpisua Belmonte JC: Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010, 464: 606–609.

Chimenti I, Smith RR, Li TS, Gerstenblith G, Messina E, Giacomello A, Marban E: Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res 2010, 106: 971–980.

Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LE, Berman D, Czer LS, Marban L, Mendizabal A, Johnston PV, et al.: Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 2012, 379: 895–904.

Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC: Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 2004, 428: 668–673.

Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, Pasumarthi KB, Virag JI, Bartelmez SH, Poppa V, et al.: Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 2004, 428: 664–668.

Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD: Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002, 105: 93–98.

Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C, Fichtner S, Korte T, Hornig B, Messinger D, et al.: Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 2004, 364: 141–148.

England TJ, Abaei M, Auer DP, Lowe J, Jones DR, Sare G, Walker M, Bath PM: Granulocyte-colony stimulating factor for mobilizing bone marrow stem cells in subacute stroke: the stem cell trial of recovery enhancement after stroke 2 randomized controlled trial. Stroke 2012, 43: 405–411.

Garg V, Garg H, Khan A, Trehanpati N, Kumar A, Sharma BC, Sakhuja P, Sarin SK: Granulocyte colony-stimulating factor mobilizes CD34(+) cells and improves survival of patients with acute-on-chronic liver failure. Gastroenterology 2012, 142: 505–512. e501

Nakajima H, Sakakibara Y, Tambara K, Marui A, Yoshimoto M, Premaratne GU, Lin X, Kanemitsu N, Sakaguchi G, Ikeda T, et al.: Delivery route in bone marrow cell transplantation should be optimized according to the etiology of heart disease. Circ J 2008, 72: 1528–1535.

Smart N, Riley PR: The stem cell movement. Circ Res 2008, 102: 1155–1168.

Kastrup J, Ripa RS, Wang Y, Jorgensen E: Myocardial regeneration induced by granulocyte-colony-stimulating factor mobilization of stem cells in patients with acute or chronic ischaemic heart disease: a non-invasive alternative for clinical stem cell therapy? Eur Heart J 2006, 27: 2748–2754.

Takano H, Ueda K, Hasegawa H, Komuro I: G-CSF therapy for acute myocardial infarction. Trends Pharmacol Sci 2007, 28: 512–517.

Fliedner TM, Graessle D, Paulsen C, Reimers K: Structure and function of bone marrow hemopoiesis: mechanisms of response to ionizing radiation exposure. Canc Biother Radiopharm 2002, 17: 405–426.

Abdou NL, Alavi JB, Abdou NI: Human bone marrow lymphocytes: B and T cell precursors and subpopulations. Blood 1976, 47: 423–430.

Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T: Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 1999, 5: 434–438.

Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM: Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999, 85: 221–228.

Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM: Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997, 275: 964–967.

Awong G, Zuniga-Pflucker JC: Thymus-bound: the many features of T cell progenitors. Front Biosci (Schol Ed) 2011, 3: 961–969.

Wojakowski W, Landmesser U, Bachowski R, Jadczyk T, Tendera M: Mobilization of stem and progenitor cells in cardiovascular diseases. Leukemia 2012, 26: 23–33.

Verfaillie CM: Adult stem cells: assessing the case for pluripotency. Trends Cell Biol 2002, 12: 502–508.

Uchida N, Jerabek L, Weissman IL: Searching for hematopoietic stem cells. II. The heterogeneity of Thy-1.1(lo)Lin(-/lo)Sca-1+ mouse hematopoietic stem cells separated by counterflow centrifugal elutriation. Exp Hematol 1996, 24: 649–659.

Uchida N, Weissman IL: Searching for hematopoietic stem cells: evidence that Thy-1.1lo Lin- Sca-1+ cells are the only stem cells in C57BL/Ka-Thy-1.1 bone marrow. J Exp Med 1992, 175: 175–184.

Lavker RM, Sun TT: Epidermal stem cells: properties, markers, and location. Proc Natl Acad Sci U S A 2000, 97: 13473–13475.

Potten CS, Loeffler M: Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 1990, 110: 1001–1020.

Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, Jaworski M, Offner S, Dunant CF, Eshkind L, Bockamp E, et al.: Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008, 135: 1118–1129.

Wojakowski W, Tendera M, Michalowska A, Majka M, Kucia M, Maslankiewicz K, Wyderka R, Ochala A, Ratajczak MZ: Mobilization of CD34/CXCR4+, CD34/CD117+, c-met+ stem cells, and mononuclear cells expressing early cardiac, muscle, and endothelial markers into peripheral blood in patients with acute myocardial infarction. Circulation 2004, 110: 3213–3220.

Wojakowski W, Tendera M, Kucia M, Zuba-Surma E, Paczkowska E, Ciosek J, Halasa M, Krol M, Kazmierski M, Buszman P, et al.: Mobilization of bone marrow-derived Oct-4+ SSEA-4+ very small embryonic-like stem cells in patients with acute myocardial infarction. J Am Coll Cardiol 2009, 53: 1–9.

Quaini F, Urbanek K, Beltrami AP, Finato N, Beltrami CA, Nadal-Ginard B, Kajstura J, Leri A, Anversa P: Chimerism of the transplanted heart. N Engl J Med 2002, 346: 5–15.

Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, Sasaki K, Shimada T, Oike Y, Imaizumi T: Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 2001, 103: 2776–2779.

Orlic D, Kajstura J, Chimenti S, Limana F, Jakoniuk I, Quaini F, Nadal-Ginard B, Bodine DM, Leri A, Anversa P: Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A 2001, 98: 10344–10349.

Hsieh PC, Segers VF, Davis ME, MacGillivray C, Gannon J, Molkentin JD, Robbins J, Lee RT: Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med 2007, 13: 970–974.

Lin SL, Li B, Rao S, Yeo EJ, Hudson TE, Nowlin BT, Pei H, Chen L, Zheng JJ, Carroll TJ, et al.: Macrophage Wnt7b is critical for kidney repair and regeneration. Proc Natl Acad Sci U S A 2010, 107: 4194–4199.

Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R, Weissman IL: A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003, 423: 409–414.

De Boer J, Wang HJ, Van Blitterswijk C: Effects of Wnt signaling on proliferation and differentiation of human mesenchymal stem cells. Tissue Eng 2004, 10: 393–401.

Ito M, Yang Z, Andl T, Cui C, Kim N, Millar SE, Cotsarelis G: Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 2007, 447: 316–320.

Greco V, Chen T, Rendl M, Schober M, Pasolli HA, Stokes N, Dela Cruz-Racelis J, Fuchs E: A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 2009, 4: 155–169.

Janssens S, Dubois C, Bogaert J, Theunissen K, Deroose C, Desmet W, Kalantzi M, Herbots L, Sinnaeve P, Dens J, et al.: Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet 2006, 367: 113–121.

Losordo DW, Henry TD, Davidson C, Sup Lee J, Costa MA, Bass T, Mendelsohn F, Fortuin FD, Pepine CJ, Traverse JH, et al.: Intramyocardial, autologous CD34+ cell therapy for refractory angina. Circ Res 2011, 109: 428–436.

Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT, Rossi MI, Carvalho AC, Dutra HS, Dohmann HJ, et al.: Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 2003, 107: 2294–2302.

Zheng XX, Sanchez-Fueyo A, Domenig C, Strom TB: The balance of deletion and regulation in allograft tolerance. Immunol Rev 2003, 196: 75–84.

Scandling JD, Busque S, Dejbakhsh-Jones S, Benike C, Millan MT, Shizuru JA, Hoppe RT, Lowsky R, Engleman EG, Strober S: Tolerance and chimerism after renal and hematopoietic-cell transplantation. N Engl J Med 2008, 358: 362–368.

Huard J, Li Y, Fu FH: Muscle injuries and repair: current trends in research. J Bone Joint Surg Am 2002, 84-A: 822–832.

Prisk V, Huard J: Muscle injuries and repair: the role of prostaglandins and inflammation. Histol Histopathol 2003, 18: 1243–1256.

Schmid P, Itin P, Cherry G, Bi C, Cox DA: Enhanced expression of transforming growth factor-beta type I and type II receptors in wound granulation tissue and hypertrophic scar. Am J Pathol 1998, 152: 485–493.

Li Y, Huard J: Differentiation of muscle-derived cells into myofibroblasts in injured skeletal muscle. Am J Pathol 2002, 161: 895–907.

Chan YS, Li Y, Foster W, Fu FH, Huard J: The use of suramin, an antifibrotic agent, to improve muscle recovery after strain injury. Am J Sports Med 2005, 33: 43–51.

Fukushima K, Badlani N, Usas A, Riano F, Fu F, Huard J: The use of an antifibrosis agent to improve muscle recovery after laceration. Am J Sports Med 2001, 29: 394–402.

Chan YS, Li Y, Foster W, Horaguchi T, Somogyi G, Fu FH, Huard J: Antifibrotic effects of suramin in injured skeletal muscle after laceration. J Appl Physiol 2003, 95: 771–780.

Hawke TJ, Garry DJ: Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 2001, 91: 534–551.

Brack AS, Conboy MJ, Roy S, Lee M, Kuo CJ, Keller C, Rando TA: Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007, 317: 807–810.

Carlson ME, Conboy IM: Loss of stem cell regenerative capacity within aged niches. Aging Cell 2007, 6: 371–382.

Ambrosio F, Ferrari RJ, Distefano G, Plassmeyer JM, Carvell GE, Deasy BM, Boninger ML, Fitzgerald GK, Huard J: The synergistic effect of treadmill running on stem-cell transplantation to heal injured skeletal muscle. Tissue Eng Part A 2010, 16: 839–849.

Dreyer HC, Blanco CE, Sattler FR, Schroeder ET, Wiswell RA: Satellite cell numbers in young and older men 24 hours after eccentric exercise. Muscle Nerve 2006, 33: 242–253.

McBride TA, Gorin FA, Carlsen RC: Prolonged recovery and reduced adaptation in aged rat muscle following eccentric exercise. Mech Ageing Dev 1995, 83: 185–200.

Jubrias SA, Esselman PC, Price LB, Cress ME, Conley KE: Large energetic adaptations of elderly muscle to resistance and endurance training. J Appl Physiol 2001, 90: 1663–1670.