Endurance exercise training promotes medullary hematopoiesis

FASEB Journal

Volumn 25, Issue 12, 2011, Pages 4348-4357

  Baker, J M ^a   De Lisio, Michael ^a   Parise, Gianni ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Blood; Bone marrow; Cytokine; Mesenchymal; Skeletal muscle

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ASSAY; CELL DIFFERENTIATION; CELL TYPE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDURANCE TRAINING; EXTRAMEDULLARY HEMATOPOIESIS; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; HISTOCHEMISTRY; MALE; MESENCHYME CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; STEM CELL; TREADMILL EXERCISE; WESTERN BLOTTING;

ANIMALS; CELL DIFFERENTIATION; CYTOKINES; ERYTHROPOIETIN; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; KIDNEY; MALE; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL ENDURANCE;

EID: 82655171631     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-189043     Document Type: Article

References (51)

1. Convertino, V. A. (1991) Blood volume: its adaptation to endurance training. Med. Sci. Sports Exerc. 23, 1338-1348
2. Malm, C., Lenkei, R., and Sjodin, B. (1999) Effects of eccentric exercise on the immune system in men. J. Appl. Physiol. 86, 461-468 (Pubitemid 29075794)
3. Pedersen, B. K., Bruunsgaard, H., Jensen, M., Toft, A. D., Hansen, H., and Ostrowski, K. (1999) Exercise and the immune system-influence of nutrition and ageing. J. Sci. Med. Sport 2, 234-252
4. Morici, G., Zangla, D., Santoro, A., Pelosi, E., Petrucci, E., Gioia, M., Bonanno, A., Profita, M., Bellia, V., Testa, U., and Bonsignore, M. R. (2005) Supramaximal exercise mobilizes hematopoietic progenitors and reticulocytes in athletes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1496-R1503 (Pubitemid 41507416)
5. Wilber, R. L. (2001) Current trends in altitude training. Sports Med. 31, 249-265
6. Pedersen, B. K., Akerström, T. C., Nielsen, A. R., and Fischer, C. P. (2007) Role of myokines in exercise and metabolism. J. Appl. Physiol. 103, 1093-1098 (Pubitemid 47358897)
7. Iwamoto, J., Takeda, T., and Ichimura, S. (2001) Effect of exercise training and detraining on bone mineral density in postmenopausal women with osteoporosis. J. Orthop. Sci. 6, 128-132 (Pubitemid 32367600)
8. Trudel, G., Payne, M., Mädler, B., Ramachandran, N., Lecompte, M., Wade, C., Biolo, G., Blanc, S., Hughson, R., Bear, L., and Uhthoff, H. K. (2009) Bone marrow fat accumulation after 60 days of bed rest persisted 1 year after activities were resumed along with hemopoietic stimulation: the Women International Space Simulation for Exploration study. J. Appl. Physiol. 107, 540-548
9. Gregory, C. A., Gunn, W. G., Peister, A., and Prockop, D. J. (2004) An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal. Biochem. 329, 77-84 (Pubitemid 38596903)
10. Sun, X., Gan, Y., Tang, T., Zhang, X., and Dai, K. (2008) In vitro proliferation and differentiation of human mesenchymal stem cells cultured in autologous plasma derived from bone marrow. Tissue Eng. A 14, 391-400
11. McKay, B.R., O'Reilly, C. E., Phillips, S. M., Tarnopolsky, M. A., and Parise, G. (2008) Co-expression of IGF-1 family members with myogenic regulatory factors following acute damaging muscle-lengthening contractions in humans. J. Physiol. 586, 5549-5560
12. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25, 402-408 (Pubitemid 34164012)
13. Shin, J. W., Lee, M. M., Son, J. Y., Lee, N. H., Cho, C. K., Chung, W. K., Cho, J. H., and Son, C. G. (2008) Myelophil, a mixture of astragali radix and salviae radix extract, moderates toxic side effects of fluorouracil in mice. World J. Gastroenterol. 14, 2323- 2328
14. Schodel, J., Klanke, B., Weidemann, A., Buchholz, B., Bernhardt, W., Bertog, M., Amann, K., Korbmacher, C., Wiesener, M., Warnecke, C., Kurtz, A., Eckardt, K. U., and Willam, C. (2009) HIF-prolyl hydroxylases in the rat kidney: physiologic expression patterns and regulation in acute kidney injury. Am. J. Pathol. 174, 1663-1674
15. Sugita, S., Kamei, Y., Oka, J., Suganami, T., and Ogawa, Y. (2007) Macrophage-colony stimulating factor in obese adipose tissue: studies with heterozygous op/+ mice. Obesity (Silver Spring) 15, 1988-1995 (Pubitemid 47407655)
16. Kim, D. H., Sandoval, D., Reed, J. A., Matter, E. K., Tolod, E. G., Woods, S. C., and Seeley, R. J. (2008) The role of GM-CSF in adipose tissue inflammation. Am. J. Physiol. Endocrinol. Metab. 295, E1038-E1046
17. Van Os, R.P., Dethmers-Ausema, B., and G. de Haan. (2008) In vitro assays for cobblestone area-forming cells, LTC-IC, and CFU-C. Methods Mol. Biol. 430, 143-157
18. Zierath, J. R., and Hawley, J. A. (2004) Skeletal muscle fiber type: influence on contractile and metabolic properties. PLoS Biol. 2, e348
19. Spivak, J. L. (2005) The anaemia of cancer: death by a thousand cuts. Nat. Rev. Cancer 5, 543-555
20. Zhang, J., Niu, C., Ye, L., Huang, H., He, X., Tong, W. G., Ross, J., Haug, J., Johnson, T., Feng, J. Q., Harris, S., Wiedemann, L. M., Mishina, Y., and Li, L. (2003) Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425, 836-841 (Pubitemid 37351467)
21. Calvi, L. M., Adams, G. B., Weibrecht, K. W., Weber, J. M., Olson, D. P., Knight, M. C., Martin, R. P., Schipani, E., Divieti, P., Bringhurst, F. R., Milner, L. A., Kronenberg, H. M., and Scadden, D. T. (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841-846 (Pubitemid 37351468)
22. Visnjic, D., Kalajzic, Z., Rowe, D. W., Katavic, V., Lorenzo, J., and Aguila, H. L. (2004) Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood 103, 3258-3264 (Pubitemid 38525648)
23. Arai, F., Hirao, A., Ohmura, M., Sato, H., Matsuoka, S., Takubo, K., Ito, K., Koh, G. Y., and Suda, T. (2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118, 149-161 (Pubitemid 38962572)
24. Yoshihara, H., Arai, F., Hosokawa, K., Hagiwara, T., Takubo, K., Nakamura, Y., Gomei, Y., Iwasaki, H., Matsuoka, S., Miyamoto, K., Miyazaki, H., Takahashi, T., and Suda T. (2007) Thrombopoietin/ MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 1, 685-697 (Pubitemid 350215333)
25. Petit, I., Szyper-Kravitz, M., Nagler, A., Lahav, M., Peled, A., Habler, L., Ponomaryov, T., Taichman, R. S., Arenzana-Seisdedos, F., Fujii, N., Sandbank, J., Zipori, D., and Lapidot, T. (2002) G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat. Immunol. 3, 687-694 (Pubitemid 34752479)
26. Gimble, J. M., Robinson, C. E., Wu, X., and Kelly, K. A. (1996) The function of adipocytes in the bone marrow stroma: an update. Bone 19, 421-428
27. Kricun, M. E. (1985) Red-yellow marrow conversion: its effect on the location of some solitary bone lesions. Skeletal Radiol. 14, 10-19
28. Tavassoli, M., Maniatis, A., and Crosby, W. H. (1974) Induction of sustained hemopoiesis in fatty marrow. Blood 43, 33-38
29. Naveiras, O., Nardi, V., Wenzel, P. L., Hauschka, P. V., Fahey, F., and Daley, G. Q. (2009) Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 460, 259-263
30. Corre, J., Barreau, C., Cousin, B., Chavoin, J. P., Caton, D., Fournial, G., Penicaud, L., Casteilla, L., and Laharrague, P. (2006) Human subcutaneous adipose cells support complete differentiation but not self-renewal of hematopoietic progenitors. J. Cell. Physiol. 208, 282-288 (Pubitemid 43993418)
31. Belaid-Choucair, Z., Lepelletier, Y., Poncin, G., Thiry, A., Humblet, C., Maachi, M., Beaulieu, A., Schneider, E., Briquet, A., Mineur, P., Lambert, C., Mendes-Da-Cruz, D., Ahui, M. L., Asnafi, V., Dy, M., Boniver, J., Nusgens, B. V., Hermine, O., and Defresne, M. P. (2008) Human bone marrow adipocytes block granulopoiesis through neuropilin-1-induced granulocyte colony-stimulating factor inhibition. Stem Cells 26, 1556-1564
32. Miharada, K. Hiroyama, T., Sudo, K., Danjo, I., Nagasawa, T., and Nakamura, Y. (2008) Lipocalin 2-mediated growth suppression is evident in human erythroid and monocyte/macrophage lineage cells. J. Cell. Physiol. 215, 526-537 (Pubitemid 351468965)
33. Yokota, T., Oritani, K., Takahashi, I., Ishikawa, J., Matsuyama, A., Ouchi, N., Kihara, S., Funahashi, T., Tenner, A. J., Tomiyama, Y., and Matsuzawa, Y. (2000) Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood 96, 1723-1732 (Pubitemid 30661055)
34. Sen, B., Xie, Z., Case, N., Ma, M., Rubin, C., and Rubin, J. (2008) Mechanical strain inhibits adipogenesis in mesenchymal stem cells by stimulating a durable beta-catenin signal. Endocrinology 149, 6065-6075
35. Simmons, C. A., Matlis, S., Thornton, A. J., Chen, S., Wang, C. Y., and Mooney, D. J. (2003) Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signal-regulated kinase (ERK1/2) signaling pathway. J. Biomech. 36, 1087-1096 (Pubitemid 36794104)
36. David, V., Martin, A., Lafage-Proust, M. H., Malaval, L., Peyroche, S., Jones, D. B., Vico, L., and Guignandon, A. (2007) Mechanical loading down-regulates peroxisome proliferator-activated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis. Endocrinology 148, 2553-6252
37. Menuki, K. Mori, T., Sakai, A., Sakuma, M., Okimoto, N., Shimizu, Y., Kunugita, N., and Nakamura, T. (2008) Climbing exercise enhances osteoblast differentiation and inhibits adipogenic differentiation with high expression of PTH/PTHrP receptor in bone marrow cells. Bone 43, 613-620
38. Grollman, W. S. (1960) Role of the kidney in erythropoiesis. Am. J. Physiol. 199, 629-632
39. Carrington, P. A, Hill, R. J., Stenberg, P. E., Levin, J., Corash, L., Schreurs, J., Baker, G., and Levin, F. C. (1991) Multiple in vivo effects of interleukin-3 and interleukin-6 on murine megakaryocytopoiesis. Blood 77, 34-41
40. Nienhuis, A. W., Donahue, R. E., Karlsson, S., Clark, S. C., Agricola, B., Antinoff, N., Pierce, J. E., Turner, P., Anderson, W. F., and Nathan, D. G. (1987) Recombinant human granulocyte- macrophage colony-stimulating factor (GM-CSF) shortens the period of neutropenia after autologous bone marrow transplantation in a primate model. J. Clin. Invest. 80, 573-577
41. Margeli, A., Skenderi, K., Tsironi, M., Hantzi, E., Matalas, A. L., Vrettou, C., Kanavakis, E., Chrousos, G., and Papassotiriou, I. (2005) Dramatic elevations of interleukin-6 and acute-phase reactants in athletes participating in the ultradistance foot race spartathlon: severe systemic inflammation and lipid and lipoprotein changes in protracted exercise. J. Clin. Endocrinol. Metab. 90, 3914-3918 (Pubitemid 41058151)
42. Bonsignore, M. R., Morici, G., Riccioni, R., Huertas, A., Petrucci, E., Veca, M., Mariani, G., Bonanno, A., Chimenti, L., Gioia, M., Palange, P., and Testa, U. (2010) Hemopoietic and angiogenetic progenitors in healthy athletes: different responses to endurance and maximal exercise. J. Appl. Physiol. 109, 60-67
43. Donnelly, S. (2001) Why is erythropoietin made in the kidney? The kidney functions as a critmeter. Am. J. Kidney. Dis. 38, 415-425
44. Rundqvist, H., Rullman, E., Sundberg, C. J., Fischer, H., Eisleitner, K., Ståhlberg, M., Sundblad, P., Jansson, E., and Gustafsson, T. (2009) Activation of the erythropoietin receptor in human skeletal muscle. Eur. J. Endocrinol. 161, 427-434
45. Steensberg, A., Keller, C., Hillig, T., Frøsig, C., Wojtaszewski, J. F., Pedersen, B. K., Pilegaard, H., and Sander, M. (2007) Nitric oxide production is a proximal signaling event controlling exercise-induced mRNA expression in human skeletal muscle. FASEB J. 21, 2683-2694 (Pubitemid 47372736)
46. Piroso, E., Erslev, A, J., Flaharty, K. K., and Caro J. (1991) Erythropoietin life span in rats with hypoplastic and hyperplastic bone marrows. Am. J. Hematol. 36, 105-110
47. Tan, C. C., Eckardt, K. U., Firth, J. D., and Ratcliffe, P. J. (1992) Feedback modulation of renal and hepatic erythropoietin mRNA in response to graded anemia and hypoxia. Am. J. Physiol. 263, p. F474-F481
48. D'Andrea, A.D., Dahl, N., Guinan, E. C., and Shimamura, A. (2002) Marrow failure. Hematology Am. Soc. Hematol. Educ. Program 2002, 58-72
49. Rozman, C., Feliu, E., Rozman, M., Reverter, J. C., Climent, C., and Berga, L. (1993) [Acquired aplastic anemia: a stereological analysis of bone marrow fatty tissue and its clinical correlations]. Med. Clin. (Barc.) 101, 441-445
50. Wingard, J. R., Hsu, J., and Hiemenz, J. W. (2010) Hematopoietic stem cell transplantation: an overview of infection risks and epidemiology. Infect. Dis. Clin. North Am. 24, 257-272
51. Broxmeyer, H. E., Orschell, C. M., Clapp, D. W., Hangoc, G., Cooper, S., Plett, P. A., Liles, W. C., Li, X., Graham-Evans, B., Campbell, T. B., Calandra, G., Bridger, G., Dale, D. C., and Srour, E. F. (2005) Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J. Exp. Med. 201, 1307-1318 (Pubitemid 40629073)