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Current Aging Science

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ISSN (Print): 1874-6098
ISSN (Online): 1874-6128

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Research Article

Growth Hormone Stimulates Murine Macrophage Migration during Aging

Author(s): Karen Steponavicius Cruz Borbely, Aldilane Lays Xavier Marques, Felipe Lima Porto, Beatriz Santana Mendonça, Salete Smaniotto and Maria Danielma dos Santos Reis*

Volume 15, Issue 3, 2022

Published on: 08 June, 2022

Page: [266 - 273] Pages: 8

DOI: 10.2174/1874609815666220415132815

Price: $65

Abstract

Background: Age-related impairments in macrophage functions have important consequences for the health of the elderly population. The aging process is also accompanied by a reduction in several hormones, including growth hormone (GH). Previous studies have shown that this hormone can affect macrophage activity in young individuals; however, the biological effects of GH stimulation on macrophages during aging have not yet been elucidated.

Objective: The aim of this work was to investigate the in vitro effects of GH on peritoneal macrophages from aged mice.

Methods: Peritoneal macrophages isolated from young (4 months-old) and old (12-15 months-old) mice were treated in vitro with 100 ng/mL of GH for 24 hours. After treatment, cells were analysed for cell morphology, reactive oxygen species (ROS) production, expression of integrins, cell adhesion to extracellular matrix molecules, and migration in transwell chambers.

Results: Although GH-treated cells from old mice exhibited decreased ROS production, we did not observe the effects of GH on macrophage morphology or macrophage phagocytic activity in young and old mice-derived cell cultures. Macrophages from old mice had increased adhesion to laminin and fibronectin substrates, as did cells obtained from young mice treated with GH, but no change was observed in the expression of integrin receptors. Furthermore, cells from old mice exhibited increased migration compared to young mice and a significant increase in macrophage migration was observed under GH stimulation.

Conclusion: Our results showed that GH can interfere with the motility of macrophages from old mice, advancing our understanding of the interactions between the immune and neuroendocrine systems during aging.

Keywords: Aging/senescence, cell adhesion, cell migration, growth factors, immunity, macrophage.

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[1]
Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007; 449(7164): 819-26.
[http://dx.doi.org/10.1038/nature06246] [PMID: 17943118]
[2]
Donato J Jr, Wasinski F, Furigo IC, Metzger M, Frazão R. Central regulation of metabolism by growth hormone. Cells 2021; 10(1): 129.
[http://dx.doi.org/10.3390/cells10010129] [PMID: 33440789]
[3]
Edwards CK III, Lorence RM, Dunham DM, et al. Hypophysectomy inhibits the synthesis of tumor necrosis factor alpha by rat macro-phages: Partial restoration by exogenous growth hormone or interferon gamma. Endocrinology 1991; 128(2): 989-86.
[http://dx.doi.org/10.1210/endo-128-2-989] [PMID: 1899224]
[4]
Tripathi A, Sodhi A. Production of nitric oxide by murine peritoneal macrophages in vitro on treatment with prolactin and growth hor-mone: Involvement of protein tyrosine kinases, Ca(++), and MAP kinase signal transduction pathways. Mol Immunol 2007; 44(12): 3185-94.
[http://dx.doi.org/10.1016/j.molimm.2007.01.024] [PMID: 17336385]
[5]
Dos Santos Reis MD, Dos Santos YMO, de Menezes CA, Borbely KSC, Smaniotto S. Resident murine macrophage migration and phago-cytosis are modulated by growth hormone. Cell Biol Int 2018; 42(5): 615-23.
[http://dx.doi.org/10.1002/cbin.10939] [PMID: 29363842]
[6]
Schneider A, Wood HN, Geden S, et al. Growth hormone-mediated reprogramming of macrophage transcriptome and effector functions. Sci Rep 2019; 9(1): 19348.
[http://dx.doi.org/10.1038/s41598-019-56017-6] [PMID: 31852980]
[7]
Bartke A. Growth hormone and aging: Updated review. World J Mens Health 2019; 37(1): 19-30.
[http://dx.doi.org/10.5534/wjmh.180018] [PMID: 29756419]
[8]
French RA, Broussard SR, Meier WA, et al. Age-associated loss of bone marrow hematopoietic cells is reversed by GH and accompanies thymic reconstitution. Endocrinology 2002; 143(2): 690-9.
[http://dx.doi.org/10.1210/endo.143.2.8612] [PMID: 11796526]
[9]
Ventevogel MS, Sempowski GD. Thymic rejuvenation and aging. Curr Opin Immunol 2013; 25(4): 516-22.
[http://dx.doi.org/10.1016/j.coi.2013.06.002] [PMID: 23831111]
[10]
Sonntag WE, Csiszar A, deCabo R, Ferrucci L, Ungvari Z. Diverse roles of growth hormone and insulin-like growth factor-1 in mammali-an aging: Progress and controversies. J Gerontol A Biol Sci Med Sci 2012; 67(6): 587-98.
[http://dx.doi.org/10.1093/gerona/gls115] [PMID: 22522510]
[11]
Son D-H, Park W-J, Lee Y-J. Recent advances in anti-aging medicine. Korean J Fam Med 2019; 40(5): 289-96.
[http://dx.doi.org/10.4082/kjfm.19.0087] [PMID: 31558007]
[12]
Tsukuba T, Yanagawa M, Okamoto K, et al. Impaired chemotaxis and cell adhesion due to decrease in several cell-surface receptors in cathepsin E-deficient macrophages. J Biochem 2009; 145(5): 565-73.
[http://dx.doi.org/10.1093/jb/mvp016] [PMID: 19174547]
[13]
Su H-W, Lanning NJ, Morris DL, Argetsinger LS, Lumeng CN, Carter-Su C. Phosphorylation of the adaptor protein SH2B1β regulates its ability to enhance growth hormone-dependent macrophage motility. J Cell Sci 2013; 126(Pt 8): 1733-43.
[http://dx.doi.org/10.1242/jcs.113050] [PMID: 23444381]
[14]
Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005; 5(12): 953-64.
[http://dx.doi.org/10.1038/nri1733] [PMID: 16322748]
[15]
Arango Duque G, Descoteaux A. Macrophage cytokines: Involvement in immunity and infectious diseases. Front Immunol 2014; 5: 491.
[http://dx.doi.org/10.3389/fimmu.2014.00491] [PMID: 25339958]
[16]
Pera A, Campos C, López N, et al. Immunosenescence: Implications for response to infection and vaccination in older people. Maturitas 2015; 82(1): 50-5.
[http://dx.doi.org/10.1016/j.maturitas.2015.05.004] [PMID: 26044074]
[17]
Yu HT, Park S, Shin E-C, Lee W-W. T cell senescence and cardiovascular diseases. Clin Exp Med 2016; 16(3): 257-63.
[http://dx.doi.org/10.1007/s10238-015-0376-z] [PMID: 26188489]
[18]
Pawelec G. Immunosenescence and cancer. Biogerontology 2017; 18(4): 717-21.
[http://dx.doi.org/10.1007/s10522-017-9682-z] [PMID: 28220304]
[19]
Lamberts SWJ, van den Beld AW, van der Lely A-J. The endocrinology of aging. Science 1997; 278(5337): 419-24.
[http://dx.doi.org/10.1126/science.278.5337.419] [PMID: 9334293]
[20]
Mazzoccoli G, Pazienza V, Piepoli A, et al. Hypothalamus-hypophysis-thyroid axis function in healthy aging. J Biol Regul Homeost Agents 2010; 24(4): 433-9.
[PMID: 21122282]
[21]
Dimitrijević M, Stanojević S, Kuštrimović N, et al. The influence of aging and estradiol to progesterone ratio on rat macrophage phenotypic profile and NO and TNF-α production. Exp Gerontol 2013; 48(11): 1243-54.
[http://dx.doi.org/10.1016/j.exger.2013.07.001] [PMID: 23850866]
[22]
Paltsev MA, Polyakova VO, Kvetnoy IM, et al. Morphofunctional and signaling molecules overlap of the pineal gland and thymus: Role and significance in aging. Oncotarget 2016; 7(11): 11972-83.
[http://dx.doi.org/10.18632/oncotarget.7863] [PMID: 26943046]
[23]
Cassado Ados A, D’Império Lima MR, Bortoluci KR. Revisiting mouse peritoneal macrophages: Heterogeneity, development, and func-tion. Front Immunol 2015; 6: 225.
[http://dx.doi.org/10.3389/fimmu.2015.00225] [PMID: 26042120]
[24]
Collado M, Serrano M. The power and the promise of oncogene-induced senescence markers. Nat Rev Cancer 2006; 6(6): 472-6.
[http://dx.doi.org/10.1038/nrc1884] [PMID: 16723993]
[25]
Muñoz-Espín D, Serrano M. Cellular senescence: From physiology to pathology. Nat Rev Mol Cell Biol 2014; 15(7): 482-96.
[http://dx.doi.org/10.1038/nrm3823] [PMID: 24954210]
[26]
Smith JR, Benghuzzi H, Tucci M, Puckett A, Hughes JL. The effects of growth hormone and insulin-like growth factor on the proliferation rate and morphology of RAW 264.7 macrophages. Biomed Sci Instrum 2000; 36: 111-6.
[PMID: 10834218]
[27]
Keane J, Tajouri L, Gray B. The effect of recombinant human growth hormone and insulin-like growth factor-1 on the mitochondrial func-tion and viability of peripheral blood mononuclear cells in vitro. Appl Physiol Nutr Metab 2015; 40(2): 105-15.
[http://dx.doi.org/10.1139/apnm-2014-0180] [PMID: 25531671]
[28]
Ferrari CKB, França EL, Monteiro LA, Santos BL, Pereira-Junior A, Honorio-França AC. Chronopharmacological effects of growth hor-mone on the executive function and oxidative stress response in rats. Iran J Basic Med Sci 2017; 20(1): 17-22.
[http://dx.doi.org/10.22038/IJBMS.2017.8087] [PMID: 28133519]
[29]
Edwards CK III, Ghiasuddin SM, Schepper JM, Yunger LM, Kelley KW. A newly defined property of somatotropin: Priming of macro-phages for production of superoxide anion. Science 1988; 239(4841 Pt 1): 769-71.
[http://dx.doi.org/10.1126/science.2829357] [PMID: 2829357]
[30]
Edwards CK III, Arkins S, Yunger LM, Blum A, Dantzer R, Kelley KW. The macrophage-activating properties of growth hormone. Cell Mol Neurobiol 1992; 12(5): 499-510.
[http://dx.doi.org/10.1007/BF00711550] [PMID: 1468117]
[31]
Simm A, Brömme H-J. Reactive oxygen species (ROS) and aging: Do we need them - can we measure them - should we block them? Signal Transduct 2005; 5(3): 115-25.
[http://dx.doi.org/10.1002/sita.200400053]
[32]
Kuka S, Tatarkova Z, Racay P, Lehotsky J, Dobrota D, Kaplan P. Effect of aging on formation of reactive oxygen species by mitochondria of rat heart. Gen Physiol Biophys 2013; 32(3): 415-20.
[http://dx.doi.org/10.4149/gpb_2013049] [PMID: 23817642]
[33]
Swift ME, Burns AL, Gray KL, DiPietro LA. Age-related alterations in the inflammatory response to dermal injury. J Invest Dermatol 2001; 117(5): 1027-35.
[http://dx.doi.org/10.1046/j.0022-202x.2001.01539.x] [PMID: 11710909]
[34]
Aprahamian T, Takemura Y, Goukassian D, Walsh K. Ageing is associated with diminished apoptotic cell clearance in vivo. Clin Exp Immunol 2008; 152(3): 448-55.
[http://dx.doi.org/10.1111/j.1365-2249.2008.03658.x] [PMID: 18422728]
[35]
Wong CK, Smith CA, Sakamoto K, Kaminski N, Koff JL, Goldstein DR. Aging impairs alveolar macrophage phagocytosis and increases influenza-induced mortality in mice. J Immunol 2017; 199(3): 1060-8.
[http://dx.doi.org/10.4049/jimmunol.1700397] [PMID: 28646038]
[36]
Warwick-Davies J, Lowrie DB, Cole PJ. Growth hormone activation of human monocytes for superoxide production but not tumor necro-sis factor production, cell adherence, or action against Mycobacterium tuberculosis. Infect Immun 1995; 63(11): 4312-6.
[http://dx.doi.org/10.1128/iai.63.11.4312-4316.1995] [PMID: 7591064]
[37]
Linehan E, Dombrowski Y, Snoddy R, Fallon PG, Kissenpfennig A, Fitzgerald DC. Aging impairs peritoneal but not bone marrow-derived macrophage phagocytosis. Aging Cell 2014; 13(4): 699-708.
[http://dx.doi.org/10.1111/acel.12223] [PMID: 24813244]
[38]
Mancuso P, McNish RW, Peters-Golden M, Brock TG. Evaluation of phagocytosis and arachidonate metabolism by alveolar macrophages and recruited neutrophils from F344xBN rats of different ages. Mech Ageing Dev 2001; 122(15): 1899-913.
[http://dx.doi.org/10.1016/S0047-6374(01)00322-0] [PMID: 11557288]
[39]
Chorro L, Geissmann F. Development and homeostasis of ‘resident’ myeloid cells: The case of the Langerhans cell. Trends Immunol 2010; 31(12): 438-45.
[http://dx.doi.org/10.1016/j.it.2010.09.003] [PMID: 21030305]
[40]
Digiacomo G, Tusa I, Bacci M, Cipolleschi MG, Dello Sbarba P, Rovida E. Fibronectin induces macrophage migration through a SFK-FAK/CSF-1R pathway. Cell Adhes Migr 2017; 11(4): 327-37.
[http://dx.doi.org/10.1080/19336918.2016.1221566] [PMID: 27588738]
[41]
Koh TJ, DiPietro LA. Inflammation and wound healing: The role of the macrophage. Expert Rev Mol Med 2011; 13(e23): e23.
[http://dx.doi.org/10.1017/S1462399411001943] [PMID: 21740602]
[42]
Kähler CM, Pischel AB, Haller T, et al. Signal transduction pathways in directed migration of human monocytes induced by human growth hormone in vitro. Int Immunopharmacol 2001; 1(7): 1351-61.
[http://dx.doi.org/10.1016/S1567-5769(01)00067-4] [PMID: 11460315]
[43]
Lins MP, de Araújo Vieira LF, Rosa AAM, Smaniotto S. Growth hormone in the presence of laminin modulates interaction of human thymic epithelial cells and thymocytes in vitro. Biol Res 2016; 49(1)
[http://dx.doi.org/10.1186/s40659-016-0097-0] [PMID: 27590178]
[44]
Messias de Lima CF, de Araújo Vieira LF, de Carvalho Wanderley LA, de Souza Ferro JN, Smaniotto S. Topical growth hormone acceler-ates wound healing in mice. Wounds 2017; 29(12): 387-92.
[PMID: 28976342]

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