Good Cop, Bad Cop: The Opposing Effects of Macrophage Activation State on Maintaining or Damaging Functional β-Cell Mass

Overview

Journal Metabolites

Publisher MDPI

Date 2020 Dec 1

PMID 33256225

Citations 13

Authors

Daelin M Jensen

Kyle V Hendricks

Austin T Mason

Jeffery S Tessem

Affiliations

Soon will be listed here.

Abstract

Loss of functional β-cell mass is a hallmark of Type 1 and Type 2 Diabetes. Macrophages play an integral role in the maintenance or destruction of pancreatic β-cells. The effect of the macrophage β-cell interaction is dependent on the activation state of the macrophage. Macrophages can be activated across a spectrum, from pro-inflammatory to anti-inflammatory and tissue remodeling. The factors secreted by these differentially activated macrophages and their effect on β-cells define the effect on functional β-cell mass. In this review, the spectrum of macrophage activation is discussed, as are the positive and negative effects on β-cell survival, expansion, and function as well as the defined factors released from macrophages that impinge on functional β-cell mass.

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References

Ward M, Li G, Hao M . Apoptotic β-cells induce macrophage reprogramming under diabetic conditions. J Biol Chem. 2018; 293(42):16160-16173. PMC: 6200952. DOI: 10.1074/jbc.RA118.004565. View

Orecchioni M, Ghosheh Y, Pramod A, Ley K . Macrophage Polarization: Different Gene Signatures in M1(LPS+) vs. Classically and M2(LPS-) vs. Alternatively Activated Macrophages. Front Immunol. 2019; 10:1084. PMC: 6543837. DOI: 10.3389/fimmu.2019.01084. View

Hughes K, Meares G, Hansen P, Corbett J . FoxO1 and SIRT1 regulate beta-cell responses to nitric oxide. J Biol Chem. 2011; 286(10):8338-8348. PMC: 3048718. DOI: 10.1074/jbc.M110.204768. View

Kamata K, Mizukami H, Inaba W, Tsuboi K, Tateishi Y, Yoshida T . Islet amyloid with macrophage migration correlates with augmented β-cell deficits in type 2 diabetic patients. Amyloid. 2014; 21(3):191-201. PMC: 4196506. DOI: 10.3109/13506129.2014.937857. View

Ginhoux F, Guilliams M . Tissue-Resident Macrophage Ontogeny and Homeostasis. Immunity. 2016; 44(3):439-449. DOI: 10.1016/j.immuni.2016.02.024. View

ONeill C, Lu C, Corbin K, Sharma P, Dula S, Carter J . Circulating levels of IL-1B+IL-6 cause ER stress and dysfunction in islets from prediabetic male mice. Endocrinology. 2013; 154(9):3077-88. PMC: 3749476. DOI: 10.1210/en.2012-2138. View

Zawalich W, Dierolf B, Zawalich K . Interleukin-1 induces time-dependent potentiation in isolated rat islets: possible involvement of phosphoinositide hydrolysis. Endocrinology. 1989; 124(2):720-6. DOI: 10.1210/endo-124-2-720. View

Efrat S . Beta-Cell Dedifferentiation in Type 2 Diabetes: Concise Review. Stem Cells. 2019; 37(10):1267-1272. DOI: 10.1002/stem.3059. View

Tessem J, Jensen J, Pelli H, Dai X, Zong X, Stanley E . Critical roles for macrophages in islet angiogenesis and maintenance during pancreatic degeneration. Diabetes. 2008; 57(6):1605-17. PMC: 2575065. DOI: 10.2337/db07-1577. View

10.

Masters S, Dunne A, Subramanian S, Hull R, Tannahill G, Sharp F . Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes. Nat Immunol. 2010; 11(10):897-904. PMC: 3103663. DOI: 10.1038/ni.1935. View

11.

Burg A, Tse H . Redox-Sensitive Innate Immune Pathways During Macrophage Activation in Type 1 Diabetes. Antioxid Redox Signal. 2017; 29(14):1373-1398. PMC: 6166692. DOI: 10.1089/ars.2017.7243. View

12.

Poltavets A, Vishnyakova P, Elchaninov A, Sukhikh G, Fatkhudinov T . Macrophage Modification Strategies for Efficient Cell Therapy. Cells. 2020; 9(6). PMC: 7348902. DOI: 10.3390/cells9061535. View

13.

Smeets S, Stange G, Leuckx G, Roelants L, Cools W, De Paep D . Evidence of Tissue Repair in Human Donor Pancreas After Prolonged Duration of Stay in Intensive Care. Diabetes. 2019; 69(3):401-412. DOI: 10.2337/db19-0529. View

14.

Burke S, Stadler K, Lu D, Gleason E, Han A, Donohoe D . IL-1β reciprocally regulates chemokine and insulin secretion in pancreatic β-cells via NF-κB. Am J Physiol Endocrinol Metab. 2015; 309(8):E715-26. PMC: 4609876. DOI: 10.1152/ajpendo.00153.2015. View

15.

Parkash J, Chaudhry M, Rhoten W . Tumor necrosis factor-alpha-induced changes in insulin-producing beta-cells. Anat Rec A Discov Mol Cell Evol Biol. 2005; 286(2):982-93. DOI: 10.1002/ar.a.20229. View

16.

Bouzakri K, Ribaux P, Tomas A, Parnaud G, Rickenbach K, Halban P . Rab GTPase-activating protein AS160 is a major downstream effector of protein kinase B/Akt signaling in pancreatic beta-cells. Diabetes. 2008; 57(5):1195-204. DOI: 10.2337/db07-1469. View

17.

Nishikoba N, Kumagai K, Kanmura S, Nakamura Y, Ono M, Eguchi H . HGF-MET Signaling Shifts M1 Macrophages Toward an M2-Like Phenotype Through PI3K-Mediated Induction of Arginase-1 Expression. Front Immunol. 2020; 11:2135. PMC: 7492554. DOI: 10.3389/fimmu.2020.02135. View

18.

Kaminski A, Kaminski E, Morgan N . Pre-incubation with interleukin-4 mediates a direct protective effect against the loss of pancreatic beta-cell viability induced by proinflammatory cytokines. Clin Exp Immunol. 2007; 148(3):583-8. PMC: 1941919. DOI: 10.1111/j.1365-2249.2007.03375.x. View

19.

Delmastro M, Piganelli J . Oxidative stress and redox modulation potential in type 1 diabetes. Clin Dev Immunol. 2011; 2011:593863. PMC: 3102468. DOI: 10.1155/2011/593863. View

20.

Gaglia J, Guimaraes A, Harisinghani M, Turvey S, Jackson R, Benoist C . Noninvasive imaging of pancreatic islet inflammation in type 1A diabetes patients. J Clin Invest. 2010; 121(1):442-5. PMC: 3007157. DOI: 10.1172/JCI44339. View