Tachykinins in the emerging immune system: Relevance to bone marrow homeostasis and maintenance of hematopoietic stem cells

Frontiers in Bioscience

Volumn 9, Issue , 2004, Pages 1782-1793

  Greco, Steven J ^a   Corcoran, Kelly E ^a   Cho, Kyung Jin ^b   Rameshwar, Pranela ^c  

^a UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^b Korea University   (South Korea)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Bone marrow; Cytokines; Hematopoiesis; Hematopoietic stem cells; Review; Tachykinins

Indexed keywords

CYTOKINE; NEUROKININ A; OXYGEN; PREPROTACHYKININ; PROTEIN P53; SUBSTANCE P; TACHYKININ DERIVATIVE; TACHYKININ RECEPTOR; TACHYKININ;

BONE MARROW; DISEASE ASSOCIATION; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; LEUKEMIA; MESENCHYME; MYELOFIBROSIS; NEUROSECRETORY CELL; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; REVIEW; ADULT; BONE MARROW CANCER; BONE MARROW CELL; CYTOLOGY; IMMUNOLOGY; MESODERM; METASTASIS; MYELOPROLIFERATIVE DISORDER; NEUROSECRETION; PHYSIOLOGY; STEM CELL; STEM CELL MOBILIZATION; STROMA CELL;

MAMMALIA; PYRONIA TITHONUS;

ADULT; BONE MARROW CELLS; BONE MARROW NEOPLASMS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL MOBILIZATION; HEMATOPOIETIC STEM CELLS; HOMEOSTASIS; HUMANS; IMMUNE SYSTEM; MESODERM; MYELOPROLIFERATIVE DISORDERS; NEUROSECRETORY SYSTEMS; RECEPTORS, TACHYKININ; STEM CELLS; STROMAL CELLS; TACHYKININS;

EID: 2442641847     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/1373     Document Type: Review

References (100)

1. Zon, L.I: Developmental biology of hematopoiesis. Blood 86, 2876 (1995)
2. Weissman, I.L: Stem Cells: units of development, units of regeneration, and units in evolution. Cell 100, 157-168 (2000)
3. Elenkov, I.J., Wilder, R.L., Chrousos G.P. and E.S. Vizi: The sympathetic nerve - an integrative interface between two supersystems: the brain and the immune system. Pharmacolog Rev 52, 595-638 (2000)
4. Moore, K.A., H. Ema and I.R. Lemischka: In vitro maintenance of highly purified, transplantable hematopoietic stem cells. Blood 89, 4337 (1997)
5. Manz, M.G., D. Traver, T. Miyamoto, I.L. Weissman and K. Akashi: Dendritic cell potentials of early lymphoid and myeloid progenitors. Blood 97, 3333 (2001)
6. Morrison, S.J., N.M. Shah and D.J. Anderson: Regulatory mechanisms in stem cell biology. Cell 88, 287 (1997)
7. Coa, Y.A., A.J. Wagers, A. Beilhack, J. Dusich, M.H. Bachmann, R.S. Negrin, I.L. Weissman, and C.H. Contag: Shifting foci of hematopoiesis during reconstitution from single stem cells. Proc Natl Acad Sci USA 101, 221-226 (2004)
8. Kaushansky, K. and A.P. Karplus: Hematopoietic growth factors: Understanding functional diversity in structural terms. Blood 82, 3229 (1993)
9. Muller-Sieburg, C.E. and E. Deryugina: The stromal cells' guide to the stem cell universe. Stem Cells 13, 477 (1995)
10. Moore, K.A., H. Ema and I.R. Lemischka: In vitro maintenance of highly purified, transplantable hematopoietic stem cells. Blood 89, 4337 (1997)
11. Dorshkind, K: Regulation of hemopoiesis by bone marrow stromal cells and their products. Annu Rev Immunol 8, 111 (1990)
12. Maestroni, G.J.M: Adrenergic regulation of haematopoiesis. Pharmacol Res 32, 249 (1995)
13. Van Hagen, P.M., E.P. Krenning, D.J. Kwekkeboom, J.C, Reubi, P.J. Anker-Lugtenburg, B. Lowenbert and S.W. Lamberts: Somatostatin and the immune and haematopoetic system: a review. Eur J Clin Invest 24, 91 (1994)
14. Rameshwar, P., A. Poddar, G. Zhu and P. Gascon: Receptor induction regulates the synergistic effects of substance P with IL-1 and PDGF on the proliferation of bone marrow fibroblasts. J Immunol 158, 3417 (1997)
15. Bischoff, S.C. and C.A. Dahinden: Effect of nerve growth factor on the release of inflammatory mediators by mature human basophils. Blood 79, 2662 (1992)
16. Tsuda, T., D. Wong, J. Dolovich, J. Bienenstock, J. Marshall and Denbury: Synergistic effects of nerve growth factor and granulocyte-macrophage colony-stimulating factor on human basophilic cell differentiation. Blood 77, 971 (1991)
17. Tordjman, R., Y. Lepelletier, V. Lemarchandel, M. Cambot, P. Gaulard, O. Hermine, & P.H. Romeo: A neuronal receptor, neuropilin-1, is essential for the initiation of the primary immune response. Nature Immunol 3, 477 (2002)
18. Mullins, M.W., J. Ciallclla, V. Rangnckar and J.P. McGillis: Characterization of a calcitonin gene-related peptide (CGRP) receptor on mouse bone marrow cells. Regulat Pep 49, 65 (1993)
19. Zbigniew, T., K. Gibson-Berry and S.Y. Felten: Noradrenergic and peptidergic innervation of the mouse femur bone marrow. Acta Histochem 98, 453 (1996)
20. DePace, D.M. and R.H. Webber: Electrostimulation and morphologic study of the nerves to the bone marrow of the albino rat. Acta Anat 93, 1 (1975)
21. Novotny, G.E.K: Direct innervation of lymphatic organs in the rat. Ann NY Acad Sci 650, 6 (1992)
22. De Leeuw, F.E., G.H. Jansen, E. Batanero, D.F. van Wichen, J. Huber and H.J. Schuurman: The neural and neuro-endocrine component of the human thymus. Brain Behav, Immunity 6, 234 (1992)
23. Foster, M.P., E. Montecino-Rodriguez, K. Dorshkind: Proliferation of bone marrow Pro-B cells is dependent on stimulation by the pituitary/Thyroid axis. J Immunol 163, 5883 (1999)
24. Webber, R.H., R, DeFelice, R.J. Ferguson and J.P. Powell: Bone marrow response to stimulation of the sympathetic trunks in rats. Acta Anat 77, 92 (1970)
25. Fras, C., P. Kravetz, D.R. Mody and M.H. Heggeness: Substance P-containing nerves within the human vertebral body: an immunohistochemical study of the basiverterbral nerve. Spine J 3, 63-67 (2003)
26. Bjurholm, A., A. Kreicberg, E. Brodin and M. Schultzberg: Substance P- and CGRP-immunoreactive nerves in bone. Peptides 9, 165-171 (1988)
27. Adamus, M.A. and Z.J. Dabrowski: Effect of the neuropeptide substance P on the rat bone marrow-derived osteogenic cells in vitro. J Cell Biochem 81, 499-506 (2001)
28. Weihe, E., D. Nohr, S. Michel, S. Muller, H.J. Zentel, T. Fink and J. Krekel: Molecular anatomy of the neuroimmune connection. Int J Neurosci 59, 1-23 (1991)
29. Goto, T., T. Yamaza, A. Mizuho and K.T. Tanaka: Light-and electron-microscopic study of the distribution of axons containing substance P and the localization of neurokinin-1 receptor in bone. Cell Tissue Res 293, 87-93 (1998)
30. Hiramoto, M., S. Aizawa, O. Iwase, M. Nakano, K. Toyama, M. Hoque, R. Nabeshima, A. Kaidow, T. Imai, H. Hoshi and H. Handa: Stimulatory effects of substance P on CD34 positive cell proliferation and differentiation in vitro are mediated by the modulation of stromal cell function. Int J Mol Med 1, 347-354 (1998)
31. Bost, K.L. and D.W. Pascual: Substance P a late-acting B lymphocyte differentiation cofactor. Am Phy Soc 262, C537 (1992)
32. Manske, J.M., E.L. Sullivan and S.M. Andersen: Substance P mediated stimulation of cytokine levels in cultured murine bone marrow stromal cells. Adv Exp Medi Biol 383, 53-64 (1995)
33. Li, Y., S.D. Douglas and W.Z. Ho: Human stem cells express substance P gene and its receptor. J Hematotherapy & Stem Cell Res 9, 445 (2000)
34. Moore, R.N., A.P. Osmand, J.A. Dunn, J.G.J.G. Joshi and B.T. Rouse: Substance P augmentation of CSF-1- stimulated in vitro myelopoiesis: a two-signal progenitor restricted, tuftsin-like effect. J Immunol 141, 2699 (1988)
35. Afan, A.M., C.S. Broome, S.E. Nicholls, A.D. Whetton and J.A. Miyan: Bone marrow innervation regulates cellular retention in the murine haemopoietic system. Br J Haematol 98, 569 (1997)
36. Nilsson, S.K., Johnston, H.M., J.A. Coverdale: Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood 97, 2293-2299 (2001)
37. Rameshwar, P., A. Poddar and P. Gascón: Hematopoietic regulation mediated by interactions among the neurokinins and cytokines. Leuk and Lymphoma 28, 1-10 (1997)
38. Rameshwar, P: Substance P: a regulatory neuropeptide for hematopoiesis and immune functions. Clin Immunol Immunopath 85, 129-133 (1997)
39. Pelletier, L., R. Angonin, J. Regnard, D. Fellmann and P. Charbord: Human bone marrow angiogenesis: in vitro modulation by substance P and neurokinin A. Br J Haematol 119, 1083-1089 (2002)
40. Afan, A.M., C.S. Broome, S.E. Nicholl, A.D. Whetton and J.A. Miyan: Bone marrow innervation regulates cellular retention in the murine haemopoietic system. Br J Haematol 98, 569 (1997)
41. Downing, J.E.G., J.A. Miyan JA: Neural immunoregulation: emerging roles for nerves in immune homeostasis and disease. Immunol Today 21, 281 (2000)
42. Anjaria, D.J., P. Rameshwar, E.A. Deitch, Xu Da- Zhong, C.A. Adams, R.M. Forsythe, J.T. Sambol, C.J. Hauser and D.H. Livingston: Hematopoietic failure following hemorrhagic shock is mediated partially through mesenteric lymph. Crit Care Med 29, 1780 (2001)
43. Bhatt, R., P. Rameshwar, K. Goldstein and Siegel: Effects of kindled seizures upon hematopoiesis in rats. Epilepsy 54, 209 (2003)
44. Iversen, P.O., N. Hjeltnes, B. Holm, T. Flatebo, I. Strom-Gundersen, W. Running, J. Stanghelle and H.B. Benestad: Depressed immunity and impaired proliferation of hematopoietic progenitor cells in patients with complete spinal cord injury. Blood 96, 2081 (2000)
45. Livingston, D.H., D. Anjaria, J. Wu, C.J. Hauser, V. Chang, E.A. Deitch and P. Rameshwar: Bone marrow failure following severe trauma in man. Annals of Surg 238, 748-753 (2003)
46. Edoff, K., M. Grenegard and C. Hildebrand: Retrograde tracing and neuropeptide immunohistochemistry of sensory neurons projecting to the cartilaginous distal femoral epiphysis of young rats. Cell & Tissue Res 299, 193 (2000)
47. Curtis, R., K.M. Adryan, Y. Zhu, P.J. Harkness, R.M. Lindsay and P.S. DiStefano: Retrograde axonal transport of ciliary neurotrophic factor is increased by peripheral nerve injury. Nature 365, 253 (1993)
48. z to the nucleus of sensory neurons. Brain Res 700, 157 (1995)
49. Johanson, S.O., M.F. Crouch and I.A. Hendry: Retrograde axonal transport of signal transduction proteins in rat sciatic nerve. Brain Res 690, 55 (1995)
50. Vass, Z., S.E. Shore, A.L. Nuttall, G. Jancso, P.B. Brechtelsbauer and J.M. Miller: Trigeminal ganglion innervation of the cochlea-A retrograde transport study. Neurosci 79, 605 (1997)
51. Tsui-Pierchala, B.A. and D.D. Ginty: Characterization of an NGF-P-TrkA retrograde-signaling complex and age- dependent regulation of TrkA phosphorylation in sympathetic neurons. J Neurosci 19, 8207 (1999)
52. Watson, F.L., H.M. Heerssen, D.B. Moheban, M.Z. Lin, C.M. Sauvageot, A. Bhattacharyya, S.L. Pomeroy and R.A. Segal: Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand- receptor complex. J Neurosci 19, 7889 (1999)
53. Satake, H., T. Kawada, K. Nomoto and H. Minakata: Insight into tachykinin-related peptides, their receptors, and invertebrate tachykinins: a review. Zoological Sci 20, 533-549 (2003)
54. Rameshwar, P. and P. Gascon: Hematopoietic modulation by the tachykinins. Acta Haematol 98, 59-64 (1997)
55. Zhang, Y., L. Lu, C. Furlonger, G.E. Wu, and C.J. Paige: Hemokinin is a hematopoietic-specific tachykinin that regulates B lymphopoiesis. Nat Immunol 1, 392-397 (2000)
56. Zimmer, G., M. Rohn, G.P. McGregor, M. Schemann, K. Conzelmann and G. Herrler: Virokinin, a bioactive peptide of the tachykinin family, is released from the fusion protein of bovine respiratory syncytial virus. J Biol Chem 278, 46854-46861 (2003)
57. Quartara, L. and C.A. Maggi: The tachykinin NK1 receptor: Part II. Distribution and pathophysiological roles. Neuropeptides 32, 1-49 (1998)
58. Donnelly, D., S. Maudsley, J.P. Gent, R.N. Moser, C.R. Hurrell and J.B.C. Findlay: Conserved polar residues in the transmembrane domain of the human tachykinin NK2 receptor: functional roles and structural implications. Biochem J 339, 55-61 (1999)
59. Ho, W.Z., J.P. Lai, X.H. Zhu, M. Uvaydova and S.D. Douglas: Human monocytes and macrophages express substance P and neurokinin1 receptor. J Immunol 159, 5654-5660 (1997)
60. van der Kleij, H.P.M., D. Ma, F.A.M. Redegeld, A.D. Kraneveld, P.P. Nijkamp and J. Bienenstock: Functional expression of neurokinin 1 receptors on mast cells induced by IL-4 and stem cell factor. J Immunol 171, 2074-2079 (2003)
61. Bandari, P.S., J. Qian, G. Yehia, H.P. Seegopaul, J.S. Harrison, P. Gascon, H. Fernandes and P. Rameshwar: Differences in the expression of neurokinin receptor in neural and bone marrow mesenchymal cells: implications for neuronal expansion from bone marrow cells. Neuropeptides 36, 13-21 (2001)
62. Rameshwar, P., H.S. Oh, C. Yook, P. Gascon and V.T. Chang: Substance P-Fibronectin-Cytokine interactions in myeloproliferative disorder with bone marrow fibrosis. Acta Haematologica 109, 1-10 (2003)
63. Bohm, S.K., E.F. Grady and N.W. Bunnett: Regulatory mechanisms that modulate signaling by G-protein-coupled receptors. Biochem J 322, 1-18 (1997)
64. Li, H., S.E. Leeman, B.E. Slack, G. Hauser, W.S. Saltsman, J.E. Krause, J.K. Blusztajn and N.D. Boyd: A substance P (neurokinin1) receptor mutant carboxyl- terminally truncated to resemble a naturally occurring receptor isoform displays enhanced responsiveness and resistance to desensitization. Proc Natl Acad Sci USA 94, 9475-9480 (1997)
65. Fong, T.M., S.A. Anderson, H. Yu, R.R. Huang and C.D. Strader: Differential activation of intracellular effecter by two isoforms of human neurokinin-1 receptor. Mol Pharmacol 41, 24-30 (1992)
66. Kyba, M. and G.Q. Daley: Hematopoiesis from embryonic stem cells: Lessons from and for ontogeny. Exp Hematol 31, 994-1006 (2003)
67. Bandari, P.S., J. Qian, H.S. Oh, J.A. Potian, G. Yehia, J.S. Harrison and P. Rameshwar: Crosstalk between neurokinin receptors is relevant to hematopoietic regulation: cloning and characterization of neurokinin2 promoter. J Neuroimmunol 138, 65-75 (2003)
68. Broome, C.S., A.D. Whetton and J.A. Miyan: Neuropeptide control of bone marrow neutrophil production is mediated by both direct and indirect effects on CFU-GM. Br J Haematol 108, 140-150 (2000)
69. Moore, R.N., A.P. Osmand, J.A. Dunn, J.G. Joshi and B.T. Rouse: Substance P augmentation of CSF-1- stimulated in vitro myelopoiesis: a two-signal progenitor restricted, tuftsin-like effect. J Immunol 141, 2699-2703 (1988)
70. Pascual, D.W., K.L. Bost, J. Xu-Amano, H. Kiyono and J.R. McGhee: The cytokine-like action of substance P upon B cell differentiation. Reg Immunol 4, 100-104 (1992)
71. Santoni, G., C. Amantini, R. Lucciarini, P. Pompei, M. Perfumi, M. Nabissi, S. Morrone and M. Picoli: Expression of substance P and its neurokinin-1 receptor on thymocytes: functional relevance in the regulation of thymocyte apoptosis and proliferation. Neuroimmunomodulation 10, 232-246 (2002-2003)
72. Zhang, Y. and C.J. Paige: T-cell developmental blockage by tachykinins antagonists and the role of hemokinin 1 in T lymphopoiesis. Blood 102, 2165-2172 (2003)
73. Dinarello, C.A: Interleukin-1 and interleukin-1 antagonism. Blood 77, 1627-1652 (1991)
74. Rameshwar, P. and P Gascón: Substance P (SP) mediates production of stem cell factor and interleukin-1 in bone marrow stroma: potential autoregulatory role for these cytokines in SP receptor expression and induction Blood 86, 482-490 (1995)
75. Joshi, D.D., A. Dang, P. Yadav, J. Qian, P.S. Bandari, K. Chen, R. Donnelly, T. Castro, P. Gascon, A. Haider and P. Rameshwar: Negative feedback on the effects of stem cell factor on hematopoiesis is partly mediated through neutral endopeptidase activity on substance P: a combined functional and proteomic study. Blood 98, 2697-2706 (2001)
76. Tripp, R.A., A. Barskey, L. Goss and L.J. Anderson: Substance P receptor expression on lymphocytes is associated with the immune response to respiratory syncytial virus infection. J Neuroimmunol 129, 141-153 (2002)
77. Kreisberg, R., M.S. Detrick and R.N. Moore: Opposing effects of tumor necrosis factor alpha and leukemia inhibitory factor in lipopolysaccharide- stimulated myelopoiesis. Infect Immun 61, 418-422 (1993)
78. Minguell, J., A. Erices and P. Connget: Mesenchymal stem cells. Exp Biol Med 226, 507-520 (2001)
79. Qian, J., K. Ramroop, A. McLeod, P.S. Bandari, D.H. Livingston, J.S. Harrison and P. Rameshwar: Induction of hypoxia-inducible factor-1α and caspase-3 in hypoxic bone marrow stroma is negatively regulated by the delayed production of substance P. J Immunol 167, 4600-4608 (2001)
80. Ho, W.Z., J.P. Lai, X.H. Zhu, M. Uvaydova and S.D. Douglas: Human monocytes and macrophages express substance P and neurokinin1 receptor. J Immunol 159, 5654-5660 (1997)
81. Rameshwar, P., D.D. Joshi, P. Yadav, P. Gascón, J. Qian, V.T. Chang, A. Anjaria, J.S. Harrison and S. Xiaosong: Mimicry between neurokinin-1 and fibronectin may explain the transport and stability of increased substance P-immunoreactivity in patients with bone marrow fibrosis. Blood 91, 3025-3031 (2001)
82. Bandari, P.S., J. Qian, G. Yehia, D.D. Joshi, P.B. Maloof, J.A. Potian, H.S. Oh, P. Gascon, J.S. Harrison and P. Rameshwar: Hematopoietic Growth Factor Inducible Neurokinin-1 type (HGFIN) gene: a transmembrane protein that is similar to neurokinin-1 interacts with substance P. Regul Peptides 111, 169-178 (2003)
83. Rameshwar, P., P. Gascon, P.S. Bandari, D.D. Joshi, A. Fernandes and A. Dang: Structural similarity between the bone marrow extracellular matrix protein and neurokinin 1 could be the limiting factor in the hematopoietic effects of substance P. Can. J Pharmacol Physiol 80, 475-481 (2002)
84. Nowicki, M. and B. Mishowiak: Substance P- a potent risk factor in childhood lymphoblastic leukaemia. Leukemia 17, 1096-1099 (2003)
85. Chow, D.C., L.A. Wenning, W.M. Miller and E.T. Papoutsakis: Modeling pO2 distributions in the bone marrow hematopoietic compartment I. Krogh's Model. Biophys J 81, 675 (2001)
86. Bianco, P.M. Riminucci, S. Gronthos and P.G. Robey: Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19, 180-192 (2001)
87. Pittenger, M.F., A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, J.D. Mosca, M.A. Moorman, D.W. Simonetti, S. Craig S and D.R. Marshak: Multilineage potential of adult human mesenchymal stem cells. Science 284, 143 (1999)
88. Potian, J.A., H. Aviv, N.M. Ponzio, J.S. Harrison and P. Rameshwar: Veto-like activity of mesenchymal stem cells (MSC): functional discrimination between cellular responses to alloantigen and recall antigens. J Immunol 171, 3426-3434 (2003)
89. Chavolla-Calderon, M., M.K. Bayer and J.P. Fontán: Bone marrow transplantation reveals an essential synergy between neuronal and hemopoietic cell neurokinin production in pulmonary inflammation. J Clin Invest 111, 973-980 (2003)
90. Katayama, I. and K. Nishioka: Substance P augments fibrogenic cytokine-induced fibroblasts proliferation: possible involvement of neuropeptide in tissue fibrosis. J Dermatol Sci 15, 201-206 (1997)
91. Harrison, J.S., P. Rameshwar, V. Chang and P. Bandari P: Oxygen saturation in the bone marrow of healthy volunteers. Blood 99, 394 (2002)
92. Oh, H.S., A. Moharita, J.G. Potian, I.P. Whitehead, J.C. Livingston, T.A. Castro, P.S. Patel, and P. Rameshwar: Bone marrow stroma influences TGF-β production in breast cancer cells to regulate c-myc activation of the preprotachykinin-I gene in breast cancer cells. Cancer Res (In press)
93. Aiuti, A., I.J. Webb, C. Bleul, T. Springer and J.C. Gutierrez-Ramos: The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J Exp Med 185, 111-120 (1997)
94. Broxmeyer, H.E: Regulation of hematopoiesis by chemokine family members. Int J Hematol 74, 9-17 (2001)
95. Christopherson, II K.W., S. Cooper, G. Hangoc and H.E. Broxmeyer: CD26 is essential for normal G-CSF- induced progenitor cell mobilization as determined by CD26-/- mice. Exp Hematol 31, 1126-1134 (2003)
96. Fiskerstrand, C.E., E. Lovejoy, L. Gerrard and J.P. Quinn: An intronic domain within the rat preprotachykinin- A gene containing a CCCT repetitive motif acts as an enhancer in differentiating embryonic stem cells. Neurosci Lett 263, 141-144 (1999)
97. Kim, H.R., S. Lavielle and S. Sagan: The two NK-1 binding sites are distinguished by one radiolabelled substance P analogue. Biochem Biophys Res Comm 306, 725-729 (2003)
98. Kondo, M., A.J. Wagers, M.G. Manz, S.S. Prohaska, D.C. Scherer, G.F. Beilhack, J.A. Shizuru and I.L. Weissman: Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu Rev Immunol 21, 759-806 (2003)
99. Bellucci, F., F. Carini, C. Catalani, P. Cucchi, A. Lecci, S. Meini, R. Patacchini, L. Quartara, R. Ricci, M. Tramontana, S. Giuliani and C.A. Maggi: Pharmacological profile of the novel mammalian tachykinin, hemokinin 1. Br J Pharmacol 135, 226-274 (2002)
100. Rupniak, N.M.J: New insights into the antidepressant actions of substance P (NK1 receptor) antagonists. Can J Physiol Pharmacol 80, 489-494 (2002)