Skip to main content

Advertisement

Log in

The role of catecholamines in mesenchymal stem cell fate

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Barry FP, Murphy JM (2004) Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36:568–584

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Caplan AI, Bruder SP (2001) Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med 7:259–264

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Chakroborty D, Sarkar C, Basu B, Dasgupta PS, Basu S (2009) Catecholamines regulate tumor angiogenesis. Cancer Res 69:3727–3730

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Cole SW, Sood AK (2012) Molecular pathways: beta-adrenergic signaling in cancer. Clin Cancer Res 18:1201–1206

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ducy P, Karsenty G (2010) The two faces of serotonin in bone biology. J Cell Biol 191:7–13

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Eberle D, Hegarty B, Bossard P, Ferré P, Foufelle F (2004) SREBP transcription factors: master regulators of lipid homeostasis. Biochimie 86:839–848

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Grills BL, Schuijers JA, Ward AR (1997) Topical application of nerve growth factor improves fracture healing in rats. J Orthop Res 15:235–242

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Harada SI, Rodan GA (2003) Control of osteoblast function and regulation of bone mass. Nature 423:349–355

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hocking AM, Gibran NS (2010) Mesenchymal stem cells: paracrine signaling and differentiation during cutaneous wound repair. Exp Cell Res 316:2213–2219

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Mignini F, Streccioni V, Amenta F (2003) Autonomic innervation of immune organs and neuroimmune modulation. Autonomic Autacoid Pharmacol 23:1–25

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • Owen M, Friedenstein AJ (1998) Stromal stem cells:marrow-derived osteogenic precursors. Ciba Found Symp 136:42–60

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Pullar CE, Manabat-Hidalgo CG, Bolaji RS, Isseroff RR (2008) β-Adrenergic receptor modulation of wound repair. Pharmacol Res 58:158–164

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Rosenbaum DM, Rasmussen SG, Kobilka BK (2009) The structure and function of G-protein-coupled receptors. Nature 459:356–363

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Sauter A, Goldstein M, Engel J, Ueta K (1983) Effect of insulin on central catecholamines. Brain Res 260:330–333

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Swierczynski J (2006) Leptin and age-related down-regulation of lipogenic enzymes genes expression in rat white adipose tissue. J Physiol Pharmacol 57:85

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Takeda S (2005) Central control of bone remodeling. Biochem Biophys Res Commun 328:697–699

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Vargovic P, Ukropec J, Laukova M (2011) Adipocytes as a new source of catecholamine production. FEBS Lett 585:2279–2284

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zweig M, Axelrod J (1969) Relationship between catecholamines and serotonin in sympathetic nerves of the rat pineal gland. J Neurobiol 1:87–97

    CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Amir Atashi or Masoud Soleimani.

Additional information

Abbas Hajifathali and Fakhredin Saba contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-014-1984-8

Keywords

Navigation