Abstract
Mesenchymal stem cells (MSCs) are multipotent stem cells found in many adult tissues, especially bone marrow (BM) and are capable of differentiation into various lineage cells such as osteoblasts, adipocytes, chondrocytes and myocytes. Moreover, MSCs can be mobilized from connective tissue into circulation and from there to damaged sites to contribute to regeneration processes. MSCs commitment and differentiation are controlled by complex activities involving signal transduction through cytokines and catecholamines. There has been an increasing interest in recent years in the neural system, functioning in the support of stem cells like MSCs. Recent efforts have indicated that the catecholamine released from neural and not neural cells could be affected characteristics of MSCs. However, there have not been review studies of most aspects involved in catecholamines-mediated functions of MSCs. Thus, in this review paper, we will try to describe the current state of catecholamines in MSCs destination and discuss strategies being used for catecholamines for migration of these cells to damaged tissues. Then, the role of the nervous system in the induction of osteogenesis, adipogenesis, chondrogenesis and myogenesis from MSCs is discussed. Recent progress in studies of signaling transduction of catecholamines in determination of the final fate of MSCs is highlighted. Hence, the knowledge of interaction between MSCs with the neural system could be applied towards the development of new diagnostic and treatment alternatives for human diseases.
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Abbreviations
- ATF4:
-
Activating transcription factor 4
- BARK:
-
β-Adr kinase
- BM:
-
Bone marrow
- BMSCs:
-
Bone marrow stem cells
- BMP4:
-
Bone morphogenetic proteins
- C/EBP:
-
CCAAT/enhancer-binding protein
- DBH:
-
Dopamine-b-Hydroxylase
- DEHP:
-
Bis (2-Ethylhexyl) phthalate
- Ebf1:
-
Early B-cell factor 1
- EPAC:
-
Exchange protein activated by adenylyl cyclase
- EPO:
-
Erythropoietin
- FGF:
-
Fibroblast growth factor
- GPC:
-
Growth plate chondrocytes
- GPCRs:
-
G-protein-coupled receptors
- GCs:
-
Glucocorticoids
- HGF:
-
Hepatocyte growth factor
- HSCs:
-
Hematopoietic stem cells
- IGF-1:
-
Insulin-like growth factor-1
- IRFs:
-
Interferon regulatory factors
- MAFbx:
-
Muscle atrophy F-box protein
- MKP-1:
-
Mitogen-activated protein kinase phosphatase
- MSCs:
-
Mesenchymal stem cells
- MuRF1:
-
Muscle ring finger1
- OGP:
-
Osteogenic growth peptide
- PB:
-
Peripheral blood
- PDEs:
-
Phosphodiesterase proteins
- PGE2:
-
Prostaglandin E2
- pRb:
-
Retinoblastoma cell cycle-related proteins
- PKA:
-
Protein kinase A
- ROS:
-
Reactive oxygen species
- SDF-1:
-
Stromal-derived factor-1
- SHH:
-
Sonic Hedgehog protein
- SNS:
-
Sympathetic nervous system
- SREBPs:
-
Sterol regulatory element binding proteins
- S1P:
-
Sphingosine1-phosphate
- TBT:
-
Tributyltin
- TB4:
-
Thymosin β
- TF:
-
Transcription factors
- TH:
-
Tyrosine hydroxylase
- TGF-β:
-
Transforming growth factor-β
- TLR-9:
-
Toll-like receptor 9
- 4EBP1:
-
eIF4E binding protein1
References
Ahmadbeigi N, Soleimani M, Vasei M, Gheisari Y, Mortazavi Y, Azadmanesh K, Omidkhoda A, Janzamin E, Nardi NB (2013) Isolation, characterization, and transplantation of bone marrow-derived cell components with hematopoietic stem cell niche properties. Stem Cells Dev 22:3052–3061
Babashah S, Sadeghizadeh M, Hajifathali A, Tavirani MR, Zomorod MS, Ghadiani M, Soleimani M (2013) Targeting of the signal transducer Smo links microRNA-326 to the oncogenic hedgehog pathway in CD34+ CML stem/progenitor cells. Int J Cancer 133:579–589
Baranski GM, Offin MD, Sifri ZC, Elhassan IO, Hannoush EJ, Alzate WD, Rameshwar P, Livingston DH, Mohr AM (2011) beta-blockade protection of bone marrow following trauma: the role of G-CSF. J Surg Res 170:325–331
Barry FP, Murphy JM (2004) Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36:568–584
Beitzel F, Gregorevic P, Ryall JG, Plant DR, Sillence M, Lynch GS (2004) β2-Adrenoceptor agonist fenoterol enhances functional repair of regenerating rat skeletal muscle after injury. J Appl Physiol 96:1385–1392
Bengtsson T, Cannon B, Nedergaard J (2000) Differential adrenergic regulation of the gene expression of the β-adrenoceptor subtypes β1, β2 and β3 in brown adipocytes. Biochem J 347:643–651
Biemann R, Navarrete Santos A, Navarrete Santos A, Riemann D, Knelangen J, Blüher M, Koch H, Fischer B (2012) Endocrine disrupting chemicals affect the adipogenic differentiation of mesenchymal stem cells in distinct ontogenetic windows. Biochem Biophys Res Commun 417:747–752
Bronnikov G, Bengtsson T, Kramarova L, Golozoubova V, Cannon B, Nedergaard J (1999) beta1 to beta3 switch in control of cyclic adenosine monophosphate during brown adipocyte development explains distinct beta-adrenoceptor subtype mediation of proliferation and differentiation. Endocrinology 140:4185–4197
Brouard N, Driessen R, Short B, Simmons PJ (2010) G-CSF increases mesenchymal precursor cell numbers in the bone marrow via an indirect mechanism involving osteoclast-mediated bone resorption. Stem Cell Res 5:65–75
Caiazzo M, Colucci-D’Amato L, Volpicelli F, Speranza L, Petrone C, Pastore L, Stifani S, Ramirez F, Bellenchi GC, di Porzio U (2011) Krüppel-like factor 7 is required for olfactory bulb dopaminergic neuron development. Exp Cell Res 317:464–473
Caplan AI, Bruder SP (2001) Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med 7:259–264
Cashen AF, Lazarus HM, Devine SM (2007) Mobilizing stem cells from normal donors: is it possible to improve upon G-CSF? Bone Marrow Transplant 39:577–588
Chakroborty D, Sarkar C, Basu B, Dasgupta PS, Basu S (2009) Catecholamines regulate tumor angiogenesis. Cancer Res 69:3727–3730
Charrier J-B, Lapointe F, Le Douarin NM, Teillet M-A (2001) Anti-apoptotic role of sonic hedgehog protein at the early stages of nervous system organogenesis. Development 128:4011–4020
Chen Z-x, Chang M, Y-l P, Zhao L, Y-r Z, L-j W, Wang R (2007) Osteogenic growth peptide C-terminal pentapeptide [OGP (10–14)] acts on rat bone marrow mesenchymal stem cells to promote differentiation to osteoblasts and to inhibit differentiation to adipocytes. Regul Pept 142:16–23
Cole SW, Sood AK (2012) Molecular pathways: beta-adrenergic signaling in cancer. Clin Cancer Res 18:1201–1206
Collino F, Bruno S, Deregibus MC, Tetta C, Camussi G (2011) MicroRNAs and mesenchymal stem cells. Vitam Horm 87:291–320
Collins S (2011) Beta-adrenoceptor signaling networks in adipocytes for recruiting stored Fat and energy expenditure. Front Endocrinol (Lausanne) 2:102
De Ugarte DA, Morizono K, Elbarbary A, Alfonso Z, Zuk PA, Zhu M, Dragoo JL, Ashjian P, Thomas B, Benhaim P, Chen I, Fraser J, Hedrick MH (2003) Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 174:101–109
Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 8:315–317
Ducy P, Karsenty G (2010) The two faces of serotonin in bone biology. J Cell Biol 191:7–13
Duncan JJ, Farr JE, Upton SJ, Hagan RD, Oglesby M, Blair SN (1985) The effects of aerobic exercise on plasma catecholamines and blood pressure in patients with mild essential hypertension. JAMA 254:2609–2613
Dygai AM, Khmelevskaya ES, Skurikhin EG, Pershina OV, Andreeva TV, Ermakova NN (2012) Catecholamine regulation of stromal precursors and hemopoietic stem cells in cytostatic myelosuppression. Bull Exp Biol Med 152:723–727
Eberle D, Hegarty B, Bossard P, Ferré P, Foufelle F (2004) SREBP transcription factors: master regulators of lipid homeostasis. Biochimie 86:839–848
Eguchi J, Yan Q-W, Schones DE, Kamal M, Hsu C-H, Zhang MQ, Crawford GE, Rosen ED (2008) Interferon regulatory factors are transcriptional regulators of adipogenesis. Cell Metab 7:86–94
Elefteriou F (2005) Neuronal signaling and the regulation of bone remodeling. Cell Mol Life Sci 62:2339–2349
Elefteriou F (2008) Regulation of bone remodeling by the central and peripheral nervous system. Arch Biochem Biophys 473:231–236
Elefteriou FAJ, Takeda S, Starbuck M, Yang X, Liu X, Kondo H, Richards WG, Bannon TW, Noda M, Clement K, Vaisse C, Karsenty G (2005) Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 434(7032):514–520
Fajas L, Egler V, Reiter R, Hansen J, Kristiansen K, Debril M-B, Miard S, Auwerx J (2002) The retinoblastoma-histone deacetylase 3 complex inhibits PPARγ and adipocyte differentiation. Dev Cell 3:903–910
Farshdousti Hagh M, Noruzinia M, Mortazavi Y, Soleimani M, Kaviani S, Mahmodinia Maymand M (2012) Zoledrinic acid induces Steoblastic differentiation of mesenchymal stem cells without change in Hypomethylation status of OSTERIX promoter. Cell J 14:90–97
Feve B, Emorine L, Lasnier F, Blin N, Baude B, Nahmias C, Strosberg A, Pairault J (1991) Atypical beta-adrenergic receptor in 3 T3-F442A adipocytes. Pharmacological and molecular relationship with the human beta 3-adrenergic receptor. J Biol Chem 266:20329–20336
Gang EJ, Jeong JA, Hong SH, Hwang SH, Kim SW, Yang IH, Ahn C, Han H, Kim H (2004) Skeletal myogenic differentiation of mesenchymal stem cells isolated from human umbilical cord blood. Stem Cells 22:617–624
Gheisari Y, Azadmanesh K, Ahmadbeigi N, Nassiri SM, Golestaneh AF, Naderi M, Vasei M, Arefian E, Mirab-Samiee S, Shafiee A, Soleimani M, Zeinali S (2012) Genetic modification of mesenchymal stem cells to overexpress CXCR4 and CXCR7 does not improve the homing and therapeutic potentials of these cells in experimental acute kidney injury. Stem Cells Dev 21:2969–2980
Grayson WL, Zhao F, Bunnell B, Ma T (2007) Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 358:948–953
Grills BL, Schuijers JA, Ward AR (1997) Topical application of nerve growth factor improves fracture healing in rats. J Orthop Res 15:235–242
Grønning LM, Baillie GS, Cederberg A, Lynch MJ, Houslay MD, Enerbäck S, Taskén K (2006) Reduced PDE4 expression and activity contributes to enhanced catecholamine-induced cAMP accumulation in adipocytes from FOXC2 transgenic mice. FEBS Lett 580:4126–4130
Guest S, Hadcock J, Watkins D, Malbon C (1990) Beta 1-and beta 2-adrenergic receptor expression in differentiating 3 T3-L1 cells. Independent regulation at the level of mRNA. J Biol Chem 265:5370–5375
Guzzo RM, Gibson J, Xu RH, Lee FY, Drissi H (2013) Efficient differentiation of human iPSC‐derived mesenchymal stem cells to chondroprogenitor cells. J Cell Biochem 114:480–490
Hall NS, O’Grady M, Steiner R, Goldstein A (1988) Interactions Between Thymosins and Neuroendocrine Circuits. In: Gorio A, Perez-Polo JR, Vellis J, Haber B (eds) Neural Development and Regeneration, vol 22, NATO ASI Series. Springer, Berlin, pp 571–582
Harada SI, Rodan GA (2003) Control of osteoblast function and regulation of bone mass. Nature 423:349–355
Hashemi SM, Hassan ZM, Pourfathollah AA, Soudi S, Shafiee A, Soleimani M (2013) In vitro immunomodulatory properties of osteogenic and adipogenic differentiated mesenchymal stem cells isolated from three inbred mouse strains. Biotechnol Lett 35:135–142
Havasi P, Nabioni M, Soleimani M, Bakhshandeh B, Parivar K (2013) Mesenchymal stem cells as an appropriate feeder layer for prolonged in vitro culture of human induced pluripotent stem cells. Mol Biol Rep 40:3023–3031
Haynesworth SE, Baber M, Caplan AI (1992) Cell surface antigens on human marrow-derived mesenchymal cells are detected by monoclonal antibodies. Bone 13:69–80
Hocking AM, Gibran NS (2010) Mesenchymal stem cells: paracrine signaling and differentiation during cutaneous wound repair. Exp Cell Res 316:2213–2219
Hu C, Yon X, Li C, Lü M, Liu D, Chen L, Hu J, Teng M, Zhang D, Fan Y (2013) CXCL12/CXCR4 axis promotes mesenchymal stem cell mobilization to burn wounds and contributes to wound repair. J Surg Res 183(1):427–434
Hwang O, Choi HJ (1995) Induction of gene expression of the catecholamine-synthesizing enzymes by insulin-like growth factor-I. J Neurochem 65:1988–1996
Ikegami D, Akiyama H, Suzuki A, Nakamura T, Nakano T, Yoshikawa H, Tsumaki N (2011) Sox9 sustains chondrocyte survival and hypertrophy in part through Pik3ca-Akt pathways. Development 138:1507–1519
Ito S, Suzuki N, Kato S, Takahashi T, Takagi M (2007) Glucocorticoids induce the differentiation of a mesenchymal progenitor cell line, ROB-C26 into adipocytes and osteoblasts, but fail to induce terminal osteoblast differentiation. Bone 40:84–92
Jang S, Kim D, Lee Y, Moon S, Oh S (2011) Modulation of sphingosine 1-phosphate and tyrosine hydroxylase in the stress-induced anxiety. Neurochem Res 36:258–267
Jeon B-J, Yang Y, Kyung Shim S, Yang H-M, Cho D, Ik Bang S (2013) Thymosin beta-4 promotes mesenchymal stem cell proliferation via an interleukin-8-dependent mechanism. Exp Cell Res 319:2526–2534
Jeschke M (2013) Pathophysiology of Burn Injury. In: Jeschke MG, Kamolz L-P, Shahrokhi S (eds) Burn Care and Treatment. Springer, Vienna, pp 13–29
Jimenez MA, Åkerblad P, Sigvardsson M, Rosen ED (2007) Critical role for Ebf1 and Ebf2 in the adipogenic transcriptional cascade. Mol Cell Biol 27:743–757
Kadivar M, Khatami S, Mortazavi Y, Shokrgozar MA, Taghikhani M, Soleimani M (2006) In vitro cardiomyogenic potential of human umbilical vein-derived mesenchymal stem cells. Biochem Biophys Res Commun 340:639–647
Katayama Y, Battista M, Kao W-M, Hidalgo A, Peired AJ, Thomas SA, Frenette PS (2006) Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124:407–421
Kawada H, Fujita J, Kinjo K, Matsuzaki Y, Tsuma M, Miyatake H, Muguruma Y, Tsuboi K, Itabashi Y, Ikeda Y (2004) Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction. Blood 104:3581–3587
Khajeniazi S, Allameh A, Soleimani M, Mortaz E (2013) Changes in COX-2 and oxidative damage factors during differentiation of human mesenchymal stem cells to hepatocyte-like cells is associated with downregulation of p53 gene. Biol Chem 394(9):1213–1222
Kim DH, Yoo KH, Choi KS, Choi J, Choi S-Y, Yang S-E, Yang Y-S, Im HJ, Kim KH, Jung HL, Sung KW, Koo HH (2005) Gene expression profile of cytokine and growth factor during differentiation of bone marrow-derived mesenchymal stem cell. Cytokine 31:119–126
Kline WO, Panaro FJ, Yang H, Bodine SC (2007) Rapamycin inhibits the growth and muscle-sparing effects of clenbuterol. J Appl Physiol 102:740–747
Koopman R, Ryall JG, Church JE, Lynch GS (2009) The role of β-adrenoceptor signaling in skeletal muscle: therapeutic implications for muscle wasting disorders. Curr Opin Clin Nutr Metab Care 12:601–606
Kumar S, Ponnazhagan S (2012) Mobilization of bone marrow mesenchymal stem cells < i > in vivo</i > augments bone healing in a mouse model of segmental bone defect. Bone 50:1012–1018
Lai LP, Mitchell J (2008a) Beta2-adrenergic receptors expressed on murine chondrocytes stimulate cellular growth and inhibit the expression of Indian hedgehog and collagen type X. J Cell Biochem 104:545–553
Lai LP, Mitchell J (2008b) β2‐adrenergic receptors expressed on murine chondrocytes stimulate cellular growth and inhibit the expression of Indian hedgehog and collagen type X. J Cell Biochem 104:545–553
Lapid K, Vagima Y, Kollet O, Lapidot T (2008) Egress and mobilization of hematopoietic stem and progenitor cells. StemBook. Harvard Stem Cell Institute, Cambridge
Lecka-Czernik B (2012) Marrow fat metabolism is linked to the systemic energy metabolism. Bone 50:534–539
Lee Y, Moujalled D, Doerflinger M, Gangoda L, Weston R, Rahimi A, de Alboran I, Herold M, Bouillet P, Xu Q (2013) CREB-binding protein (CBP) regulates β-adrenoceptor (β-AR)-mediated apoptosis. Cell Death Differ 20:941–952
Li H, Fong C, Chen Y, Cai G, Yang M (2010a) β2- and β3-, but not β1-adrenergic receptors are involved in osteogenesis of mouse mesenchymal stem cells via cAMP/PKA signaling. Royaume 496:77–83
Li H, Fong C, Chen Y, Cai G, Yang M (2010b) Beta-adrenergic signals regulate adipogenesis of mouse mesenchymal stem cells via cAMP/PKA pathway. Mol Cell Endocrinol 323:201–207
Li H, Fong CC, Chen Y, Cai G, Yang M (2012) Imipramine inhibits adipogenic differentiation in both 3 T3-L1 preadipocytes and mouse marrow stromal cells. J Genet Genomics 39:173–180
Lindroos PM, Zarnegar R, Michalopoulos GK (1991) Hepatocyte growth factor (hepatopoietin A) rapidly increases in plasma before DNA synthesis and liver regeneration stimulated by partial hepatectomy and carbon tetrachloride administration. Hepatology 13:743–750
Linsley C, Wu B, Tawil B (2013) The effect of fibrinogen, collagen type I, and fibronectin on mesenchymal stem cell growth and differentiation into osteoblasts. Tissue Eng A 19:1416–1423
Liu R, Birke O, Morse A, Peacock L, Mikulec K, Littele DG, Schindeler A (2011) Myogenic progenitors contribute to open but not closed fracture repair.BMC Musculoskel Disord 12:288
Lynch GS, Ryall JG (2008) Role of β-adrenoceptor signaling in skeletal muscle: implications for muscle wasting and disease. Physiol Rev 88:729–767
Mabvuure N, Hindocha S, Jordan D, Khan WS (2012) Chondrogenesis and developments in our understanding. Curr Stem Cell Res Ther 7:243–259
Maina F, Hilton MC, Andres R, Wyatt S, Klein R, Davies AM (1998) Multiple roles for hepatocyte growth factor in sympathetic neuron development. Neuron 20:835–846
Mano T, Nishimura N, Iwase S (2010) Sympathetic neural influence on bone metabolism in microgravity (review). Acta Physiol Hung 97:354–361
Markowski DN, Helmke BM, Meyer F, von Ahsen I, Nimzyk R, Nolte I, Bullerdiek J (2011) BMP4 increases expression of HMGA2 in mesenchymal stem cells. Cytokine 56:811–816
Masur K, Niggemann B, Zanker KS, Entschladen F (2001) Norepinephrine-induced migration of SW 480 colon carcinoma cells is inhibited by β-blockers. Cancer Res 61:2866–2869
Mignini F, Streccioni V, Amenta F (2003) Autonomic innervation of immune organs and neuroimmune modulation. Autonomic Autacoid Pharmacol 23:1–25
Minkowitz B, Boskey A, Lane JM, Pearlman HS, Vigorita VJ (1991) Effects of propranolol on bone metabolism in the rat. J Orthop Res 9:869–875
Morisco C, Zebrowski DC, Vatner DE, Vatner SF, Sadoshima J (2001) β-Adrenergic cardiac hypertrophy is mediated primarily by the β1subtype in the rat heart. J Mol Cell Cardiol 33:561–573
Nadri S, Soleimani M, Hosseni RH, Massumi M, Atashi A, Izadpanah R (2007) An efficient method for isolation of murine bone marrow mesenchymal stem cells. Int J Dev Biol 51:723–729
Nadri S, Soleimani M, Mobarrae Z, Aminia S (2008) Expression of dopamine-associated genes on conjunctiva stromal-derived human mesenchymal stem cells. Biochem Biophys Res Commun 377:423–428
Nedergaard J, Herron D, Jacobsson A, Rehnmark S, Cannon B (1995) Norepinephrine as a morphogen?: its unique interaction with brown adipose tissue. Int J Dev Biol 39:827–837
Negishi M, Ito S (1992) Prostaglandin E2-induced arachidonic acid release and catecholamine secretion from cultured bovine adrenal chromaffin cells. Biochem Pharmacol 44:2315–2321
Ninomiya T, Hosoya A, Hiraga T, Koide M, Yamaguchi K, Oida H, Arai Y, Sahara N, Nakamura H, Ozawa H (2011) Prostaglandin E2 receptor EP4-selective agonist (ONO-4819) increases bone formation by modulating mesenchymal cell differentiation. Eur J Pharmacol 650:396–402
Nogami M, Romberger DJ, Rennard SI, Toews ML (1994) TGF-beta 1 modulates beta-adrenergic receptor number and function in cultured human tracheal smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 266:L187–L191
Nurmenniemi S, Kuvaja P, Lehtonen S, Tiuraniemi S, Alahuhta I, Mattila RK, Risteli J, Salo T, Selander KS, Nyberg P, Lehenkari P (2010) Toll-like receptor 9 ligands enhance mesenchymal stem cell invasion and expression of matrix metalloprotease-13. Exp Cell Res 316:2676–2682
Ostrowski SR, Pedersen SH, Jensen JS, Mogelvang R, Johansson PI (2013) Acute myocardial infarction is associated with endothelial glycocalyx and cell damage and a parallel increase in circulating catecholamines. Crit Care 17:R32
Owen M, Friedenstein AJ (1998) Stromal stem cells:marrow-derived osteogenic precursors. Ciba Found Symp 136:42–60
Path G, Bornstein SR, Gurniak M, Chrousos GP, Scherbaum WA, Hauner H (2001) Human breast adipocytes express interleukin-6 (IL-6) and its receptor system: increased IL-6 production by beta-adrenergic activation and effects of IL-6 on adipocyte function. J Clin Endocrinol Metab 86:2281–2288
Peng H, Myers J, Fang X, Stachowiak EK, Maher PA, Martins GG, Popescu G, Berezney R, Stachowiak MK (2002) Integrative nuclear FGFR1 signaling (INFS) pathway mediates activation of the tyrosine hydroxylase gene by angiotensin II, depolarization and protein kinase C. J Neurochem 81:506–524
Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, Ponomaryov T, Taichman RS, Arenzana-Seisdedos F, Fujii N, Sandbank J, Zipori D, Lapidot T (2002) G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 3:687–694
Pierroz DD, BP, Bouxsein ML, Ferrari SL (2006) Low cortical bone mass in mice lacking beta 1 and beta 2 adrenergic receptors is associated with low bone formation and circulating IGF-1. J Bone Miner Res 21:(Suppl.1):S277
Pittenger MF, Mackay A, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147
Porse BT, Pedersen TÅ, Xu X, Lindberg B, Wewer UM, Friis-Hansen L, Nerlov C (2001) E2F repression by C/EBPα is required for adipogenesis and granulopoiesis in vivo. Cell 107:247–258
Pullar CE, Manabat-Hidalgo CG, Bolaji RS, Isseroff RR (2008) β-Adrenergic receptor modulation of wound repair. Pharmacol Res 58:158–164
Qiu W, Chen L, Kassem M (2011) Activation of non-canonical Wnt/JNK pathway by Wnt3a is associated with differentiation fate determination of human bone marrow stromal (mesenchymal) stem cells. Biochem Biophys Res Commun 413:98–104
Ranjit S, Boutet E, Gandhi P, Prot M, Tamori Y, Chawla A, Greenberg AS, Puri V, Czech MP (2011) Regulation of fat specific protein 27 by isoproterenol and TNF-alpha to control lipolysis in murine adipocytes. J Lipid Res 52:221–236
Rehnmark S, Nechad M, Herron D, Cannon B, Nedergaard J (1990) Alpha-and beta-adrenergic induction of the expression of the uncoupling protein thermogenin in brown adipocytes differentiated in culture. J Biol Chem 265:16464–16471
Rejnmark L, Vestergaard P, Kassem M, Christoffersen BR, Kolthoff N, Brixen K, Mosekilde L (2004) Fracture risk in perimenopausal women treated with beta-blockers. Calcif Tissue Int 75:365–372
Richter S, Qin N, Pacak K,Eisenhofer G (2013) Chapter Fourteen - Role of Hypoxia and HIF2α in Development of the Sympathoadrenal Cell Lineage and Chromaffin Cell Tumors with Distinct Catecholamine Phenotypic Features. In: Lee EE (ed) Advances in Pharmacology, vol 68. Academic, New York, p 285–317
Robertson D, Krantz SB, Biaggioni I (1994) The anemia of microgravity and recumbency: role of sympathetic neural control of erythropoietin production. Acta Astronaut 33:137–141
Rosenbaum DM, Rasmussen SG, Kobilka BK (2009) The structure and function of G-protein-coupled receptors. Nature 459:356–363
Ryall JG, Lynch GS (2008) The potential and the pitfalls of β-adrenoceptor agonists for the management of skeletal muscle wasting. Pharmacol Ther 120:219–232
Ryall JG, Church JE, Lynch GS (2010) Novel role for β‐adrenergic signalling in skeletal muscle growth, development and regeneration. Clin Exp Pharmacol Physiol 37:397–401
Saba F, Soleimani M, Atashi A, Mortaz E, Shahjahani M, Roshandel E, Jaseb K, Saki N (2013) The role of the nervous system in hematopoietic stem cell mobilization. Lab Hematol 19:8–16
Saki N, Abroun S, Farshdousti Hagh M, Asgharei F (2011) Neoplastic bone marrow niche: hematopoietic and mesenchymal stem cells. Cell J (Yakhteh) 13:131–136
Sarkar C, Chakroborty D, Basu S (2013) Neurotransmitters as regulators of tumor angiogenesis and immunity: the role of catecholamines. J Neuroimmune Pharmacol 8:7–14
Sato S, Hanada R, Kimura A, Abe T, Matsumoto T, Iwasaki M, Inose H, Ida T, Mieda M, Takeuchi Y (2007) Central control of bone remodeling by neuromedin U. Nat Med 13:1234–1240
Sauter A, Goldstein M, Engel J, Ueta K (1983) Effect of insulin on central catecholamines. Brain Res 260:330–333
Semerad CL, Christopher MJ, Liu F, Short B, Simmons PJ, Winkler I, Levesque JP, Chappel J, Ross FP, Link DC (2005) G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood 106:3020–3027
Shiota M, Heike T, Haruyama M, Baba S, Tsuchiya A, Fujino H, Kobayashi H, Kato T, Umeda K, Yoshimoto M (2007) Isolation and characterization of bone marrow-derived mesenchymal progenitor cells with myogenic and neuronal properties. Exp Cell Res 313:1008–1023
Shizukuda Y, Buttrick PM (2002) Subtype specific roles of β-adrenergic receptors in apoptosis of adult rat ventricular myocytes. J Mol Cell Cardiol 34:823–831
Shome S, Dasgupta PS, Basu S (2012) Dopamine regulates mobilization of mesenchymal stem cells during wound angiogenesis. PLoS ONE 7:e31682
Silva WA, Covas DT, Panepucci RA, Proto-Siqueira R, Siufi JL, Zanette DL, Santos AR, Zago MA (2003) The profile of gene expression of human marrow mesenchymal stem cells. Stem Cells 21:661–669
Sneddon A, Delday M, Steven J, Maltin C (2001) Elevated IGF-II mRNA and phosphorylation of 4E-BP1 and p70S6k in muscle showing clenbuterol-induced anabolism. Am J Physiol-Endocrinol Metab 281:E676–E682
Soleimani M, Nadri S, Shabani I (2010) Neurogenic differentiation of human conjunctiva mesenchymal stem cells on a nanofibrous scaffold. Int J Dev Biol 54:1295–1300
Soleimani M, Abbasnia E, Fathi M, Sahraei H, Fathi Y, Kaka G (2012) The effects of low-level laser irradiation on differentiation and proliferation of human bone marrow mesenchymal stem cells into neurons and osteoblasts–an in vitro study. Lasers Med Sci 27:423–430
Song C, Li G (2011) CXCR4 and matrix metalloproteinase-2 are involved in mesenchymal stromal cell homing and engraftment to tumors. Cytotherapy 13:549–561
Srivastava S, Bedi U, Roy P (2012) Synergistic actions of insulin-sensitive and Sirt1-mediated pathways in the differentiation of mouse embryonic stem cells to osteoblast. Mol Cell Endocrinol 361:153–164
Stanojević S, Dimitrijević M, Kuštrimović N, Mitić K, Vujić V, Leposavić G (2013) Adrenal hormone deprivation affects macrophage catecholamine metabolism and β2-adrenoceptor density, but not propranolol stimulation of tumour necrosis factor-α production. Exp Physiol 98:665–678
Sun X, Ng YC (1998) Effects of norepinephrine on expression of IGF-1/IGF-1R and SERCA2 in rat heart. Cardiovasc Res 37:202–209
Sun X, Gao X, Zhou L, Sun L, Lu C (2013) PDGF-BB-induced MT1-MMP expression regulates proliferation and invasion of mesenchymal stem cells in 3-dimensional collagen via MEK/ERK1/2 and PI3K/AKT signaling. Cell Signal 25:1279–1287
Suzuki A, Palmer G, Bonjour J-P, Caverzasio J (1998) Catecholamines stimulate the proliferation and alkaline phosphatase activity of MC3T3-E1 osteoblast-like cells. Bone 23:197–203
Swierczynski J (2006) Leptin and age-related down-regulation of lipogenic enzymes genes expression in rat white adipose tissue. J Physiol Pharmacol 57:85
Takarada T, Hojo H, Iemata M, Sahara K, Kodama A, Nakamura N, Hinoi E, Yoneda Y (2009) Interference by adrenaline with chondrogenic differentiation through suppression of gene transactivation mediated by Sox9 family members. Bone 45:568–578
Takeda S (2005) Central control of bone remodeling. Biochem Biophys Res Commun 328:697–699
Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, Parker KL, Armstrong D, Ducy P, Karsenty G (2002) Leptin regulates bone formation via the sympathetic nervous system. Cell 111:305–317
Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD (2002) Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105:93–98
Tormos Kathryn V, Anso E, Hamanaka Robert B, Eisenbart J, Joseph J, Kalyanaraman B, Chandel Navdeep S (2011) Mitochondrial complex III ROS regulate adipocyte differentiation. Cell Metab 14:537–544
Tsang DP, Cheng AS (2011) Epigenetic regulation of signaling pathways in cancer: role of the histone methyltransferase EZH2. J Gastroenterol Hepatol 26:19–27
Udelsman R, Goldstein DS, Loriaux DL, Chrousos GP (1987) Catecholamine-glucocorticoid interactions during surgical stress. J Surg Res 43:539–545
Uemura T, Ohta Y, Nakao Y, Manaka T, Nakamura H, Takaoka K (2010) Epinephrine accelerates osteoblastic differentiation by enhancing bone morphogenetic protein signaling through a cAMP/protein kinase a signaling pathway. Bone 47:756–765
Vargovic P, Ukropec J, Laukova M (2011) Adipocytes as a new source of catecholamine production. FEBS Lett 585:2279–2284
Varley JE, Maxwell GD (1996) BMP-2 and BMP-4, but Not BMP-6, increase the number of adrenergic cells which develop in quail trunk neural crest cultures. Exp Neurol 140:84–94
Vashisht R, Sian M, Franks PJ, O’Malley MK (1992) Long-term reduction of intimal hyperplasia by the selective alpha-1 adrenergic antagonist doxazosin. Br J Surg 79:1285–1288
Vogel S, Peters C, Etminan N, Börger V, Schimanski A, Sabel MC, Sorg RV (2013) Migration of mesenchymal stem cells towards glioblastoma cells depends on hepatocyte-growth factor and is enhanced by aminolaevulinic acid-mediated photodynamic treatment. Biochem Biophys Res Commun 431:428–432
Weiss DR, Ahn S, Sassano MF, Kleist A, Zhu X, Strachan R, Roth BL, Lefkowitz RJ, Shoichet BK (2013) Conformation guides molecular efficacy in docking screens of activated β-2 adrenergic G protein coupled receptor. ACS Chem Biol 8:1018-1026
Xiao G, Jiang D, Ge C, Zhao Z, Lai Y, Boules H, Phimphilai M, Yang X, Karsenty G, Franceschi RT (2005) Cooperative interactions between activating transcription factor 4 and Runx2/Cbfa1 stimulate osteoblast-specific osteocalcin gene expression. J Biol Chem 280:30689–30696
Xiao R-P, Zhu W, Zheng M, Cao C, Zhang Y, Lakatta EG, Han Q (2006) Subtype-specific α1 and β-adrenoceptor signaling in the heart. Trends Pharmacol Sci 27:330–337
Xinaris C, Morigi M, Benedetti V, Imberti B, Fabricio A, Squarcina E, Benigni A, Gagliardini E, Remuzzi G (2013) A novel strategy to enhance mesenchymal stem cell migration capacity and promote tissue repair in an injury specific fashion. Cell Transplant 22:423–436
Xue P, Wu X, Zhou L, Ma H, Wang Y, Liu Y, Ma J, Li Y (2013) IGF1 promotes osteogenic differentiation of mesenchymal stem cells derived from rat bone marrow by increasing TAZ expression. Biochem Biophys Res Commun 433:226–231
Yang EV, Sood AK, Chen M, Li Y, Eubank TD, Marsh CB, Jewell S, Flavahan NA, Morrison C, Yeh PE, Lemeshow S, Glaser R (2006) Norepinephrine up-regulates the expression of vascular endothelial growth factor, matrix metalloproteinase (MMP)-2, and MMP-9 in nasopharyngeal carcinoma tumor cells. Cancer Res 66:10357–10364
Yazdani SO, Hafizi M, Zali AR, Atashi A, Ashrafi F, Seddighi AS, Soleimani M (2013) Safety and possible outcome assessment of autologous Schwann cell and bone marrow mesenchymal stromal cell co-transplantation for treatment of patients with chronic spinal cord injury. Cytotherapy 15:782–791
Yousefi F, Ebtekar M, Soleimani M, Soudi S, Hashemi SM (2013) Comparison of in vivo immunomodulatory effects of intravenous and intraperitoneal administration of adipose-tissue mesenchymal stem cells in experimental autoimmune encephalomyelitis (EAE). Int Immunopharmacol 17:608–616
Yu K, Xu J, Liu Z, Sosic D, Shao J, Olson EN, Towler DA, Ornitz DM (2003) Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130:3063–3074
Yu X, Chen D, Zhang Y, Wu X, Huang Z, Zhou H, Zhang Y, Zhang Z (2012) Overexpression of CXCR4 in mesenchymal stem cells promotes migration, neuroprotection and angiogenesis in a rat model of stroke. J Neurol Sci 316:141–149
Zaugg M, Xu W, Lucchinetti E, Shafiq SA, Jamali NZ, Siddiqui M (2000) β-Adrenergic receptor subtypes differentially affect apoptosis in adult rat ventricular myocytes. Circulation 102:344–350
Zhao L, Hantash BM (2011) TGF-β1 regulates differentiation of bone marrow mesenchymal stem cells. In: Gerald L (ed) Vitamins and Hormones, vol 87. Academic, New York, p 127–141
Zhu XH, He QL, Lin ZH (2003) Effect of catecholamines on human preadipocyte proliferation and differentiation. Zhongua Xing Wai Ke Za Zhi 19:282–284
Zisa D, Shabbir A, Suzuki G, Lee T (2009) Vascular endothelial growth factor (VEGF) as a key therapeutic trophic factor in bone marrow mesenchymal stem cell-mediated cardiac repair. Biochem Biophys Res Commun 390:834–838
Zuk PA, Zhu M, Ashjian P et al (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295
Zweig M, Axelrod J (1969) Relationship between catecholamines and serotonin in sympathetic nerves of the rat pineal gland. J Neurobiol 1:87–97
Acknowledgments
We would like to acknowledge Thomas J. Kelly for his revisions and thank all our colleagues at the Department of Hematology in Tarbiat Modares University for assistance with the manuscript. This study was supported by Tarbiat Modares University.
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Abbas Hajifathali and Fakhredin Saba contributed equally to this work.
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Hajifathali, A., Saba, F., Atashi, A. et al. The role of catecholamines in mesenchymal stem cell fate. Cell Tissue Res 358, 651–665 (2014). https://doi.org/10.1007/s00441-014-1984-8
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DOI: https://doi.org/10.1007/s00441-014-1984-8