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Early Microvascular Dysfunction: Is the Vasa Vasorum a “Missing Link” in Insulin Resistance and Atherosclerosis

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Early Microvascular Dysfunction: Is the Vasa Vasorum a “Missing Link” in Insulin Resistance and Atherosclerosis International Journal of Molecular Sciences Review Early Microvascular Dysfunction: Is the Vasa Vasorum a “Missing Link” in Insulin Resistance and Atherosclerosis Jeanette Owusu 1 and Eugene Barrett 1,2,3,* 1 Department of Medicine, School of Medicine, University of Virginia, Charlottesville, VA 22908, USA; [email protected] 2 Department of Pediatrics, School of Medicine, University of Virginia, Charlottesville, VA 22908, USA 3 Department of Pharmacology, School of Medicine, University of Virginia, Charlottesville, VA 22908, USA * Correspondence: [email protected]; Tel.: +1-434-924-1263 Abstract: The arterial vasa vasorum is a specialized microvasculature that provides critical perfusion required for the health of the arterial wall, and is increasingly recognized to play a central role in atherogenesis. Cardio-metabolic disease (CMD) (including hypertension, metabolic syndrome, obesity, diabetes, and pre-diabetes) is associated with insulin resistance, and characteristically injures the microvasculature in multiple tissues, (e.g., the eye, kidney, muscle, and heart). CMD also increases the risk for atherosclerotic vascular disease. Despite this, the impact of CMD on vasa vasorum structure and function has been little studied. Here we review emerging information on the early impact of CMD on the microvasculature in multiple tissues and consider the potential impact on atherosclerosis development and progression, if vasa vasorum is similarly affected. Keywords: atherosclerosis; adventitial vasa vasorum; microvascular insulin resistance; angiogenesis Citation: Owusu, J.; Barrett, E. Early Microvascular Dysfunction: Is the Vasa Vasorum a “Missing 1. Introduction Link” in Insulin Resistance and The vasa vasorum is the nexus of the micro- and macro-vasculature and as such forms Atherosclerosis. Int. J. Mol. Sci. 2021, a nidus where dysfunction of, or injury to, either element may impact the integrity of the 22, 7574. https://doi.org/10.3390/ other, setting off a chain reaction that could accelerate vascular disease development. It is ijms22147574 both curious and unfortunate that for cardio-metabolic disease (CMD), which adversely affects both the micro- and macro-vasculature, the involvement of vasa vasorum has been Academic Editor: Anna Solini little studied. In contrast, the impact of insulin resistance, hypertension, and diabetes on microvascular structure and function has been extensively studied in multiple tissues Received: 9 June 2021 other than the arterial wall. We focus this brief review on the potential for significant Accepted: 10 July 2021 Published: 15 July 2021 parallels between findings in the vasa vasorum and microvasculature at other tissue sites. We also briefly review data indicating a central role for vasa vasorum in the pathogen- esis of atherosclerotic lesions and the acceleration of that process by insulin resistance Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in and diabetes. published maps and institutional affil- 2. Structure and Function of the Arterial Vasa Vasorum iations. Before addressing vasa vasorum pathophysiology, we briefly review its normal struc- ture and function. The arterial vasa vasorum refers to the network of arterioles, capillaries and small venules that enter and supply the arterial wall from either the luminal (vasa vasorum interna) or (much more abundantly) from the adventitial (vasa vasorum externa, Copyright: © 2021 by the authors. or adventitial vasa vasorum) surface (Figure1). The tunica intima of larger arteries is a Licensee MDPI, Basel, Switzerland. This article is an open access article thin band comprised of the endothelium with its basement membrane, occasional pericytes distributed under the terms and and adjacent connective tissue that encircles the lumen and bounded by the internal elastic conditions of the Creative Commons lamina. It is nourished directly by diffusion of oxygen and nutrients from within the Attribution (CC BY) license (https:// arterial lumen. Within the tunica media of the vessel wall, elastin and collagen elements as creativecommons.org/licenses/by/ well as smooth muscle cells (SMC) are arranged in an orderly, stacked, lamellar pattern. 4.0/). Generally, arteries with a lumen diameter < 0.5 mm, or a wall thickness < 29 medial lamellar Int. J. Mol. Sci. 2021, 22, 7574. https://doi.org/10.3390/ijms22147574 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 10 Int. J. Mol. Sci. 2021, 22, 7574 2 of 10 elements as well as smooth muscle cells (SMC) are arranged in an orderly, stacked, lamel- lar pattern. Generally, arteries with a lumen diameter < 0.5 mm, or a wall thickness < 29 medialunits [1 lamellar,2] have nounits vasa [1,2] vasorum. have no The vasa media vasorum. of these The smaller media arterial of these vessels, smaller like arterial the intima ves- sels,of larger like the vessels, intima receives of larger oxygen vessels, and receives nutrient oxygen exchange and nutrient directly fromexchange the arterial directly lumen. from theFor arterial the media lumen. of large For arterialthe media vessels, of large the bloodarterial carried vessels, through the blood the vasa carried vasorum, through arising the vasafrom vasorum, the adventitia, arising provides from the gas adventitia, and nutrient provides exchange gas and with nutrient the cellular exchange components, with the cellularmostly components, SMC, fibroblasts, mostly and SMC, sympathetic fibroblast nerves, and processes. sympathetic The nerve adventitial processes. layer The of ad- the ventitialvasa vasorum layer of extends the vasa outward vasorum from extends the external outward elastic from membrane the external of the elastic vessel membrane wall and ofincludes the vessel connective wall and tissue includes elements connective (fibroblasts, tissue adipocytes, elements (fibroblasts, and pre-adipocytes, adipocytes, elastin, and pre-adipocytes,collagen), as well elastin, as macrophages collagen), as and well leukocytes. as macrophages The vasa and vasorumleukocytes. externa The vasa arises vaso- off rumbranches externa of parentarises arteries,off branches investing of parent first the arteries, arterial investing adventitia first and the proceeding arterial adventitia inward to andthe arterialproceeding media. inward to the arterial media. FigureFigure 1. 1. MostMost microvessels microvessels of of the the vasa vasa vasorum vasorum enter enter the the vessel vessel wall wall from from the the adventitial adventitial layer layer wherewhere they they tend tend to to course course longitudinally longitudinally along along th thee vessel vessel axis. axis. After After penetrating penetrating to to the the media media of of the the arterialarterial wall wall they they more more typically typically orient orient circumfere circumferentiallyntially through through the the media. media. Much Much less less abundant abundant is theis the vasa vasa vasorum vasorum interna interna with with its its short short vessels vessels fe feedingeding small small areas areas of of the the innermost innermost third third of of the the vessel wall. vessel wall. InIn humans, humans, the the vasa vasa vasorum vasorum is is present present in in the the walls walls of of many many larger larger arterial arterial vessels vessels includingincluding the the coronary coronary arteries, arteries, the the aorta aorta and and its branches, its branches, (subclavian, (subclavian, carotid, carotid, iliac, fem- iliac, oralfemoral and brachial) and brachial) and the and intercostal the intercostal arteries arteries branching branching off the off descending the descending thoracic thoracic aorta [3].aorta Anatomically, [3]. Anatomically, there is there the isfirst the order first order vasa vasawhich which runs runslongitudinally longitudinally between between the ad- the ventitiaadventitia and and media media paralleling paralleling the the lumen lumen while while second second order order vasa vasa run run circumferentially circumferentially aroundaround the the vessel vessel and and often often penetrates penetrates into into the the tunica tunica media. media. SmallSmall laboratory laboratory rodents rodents (rats, (rats, mice) mice) normally normally lack lack vasa vasa vasorum vasorum in their in their arterial arterial ves- selsvessels [3], however, [3], however, vascular vascular injury injury or athero orgenesis atherogenesis in genetically in genetically prone laboratory prone laboratory rodents eachrodents can eachpromote can formation promote formationof a reactive, of amore reactive, inflammatory more inflammatory “neovascular” “neovascular” vasa vaso- rumvasa at vasorum sites of pathologic at sites of injury. pathologic Development injury. Development of this usually of begins this usually from vessels begins in from the adventitialvessels in layer the adventitial which, as noted, layer which,includes as no noted,t just vessels includes but not resident just vessels macrophages, but resident mast cells,macrophages, B and T-lymphocytes, mast cells, B adipocytes, and T-lymphocytes, fibroblasts, adipocytes, and progenitor fibroblasts, cells. In and non-diseased progenitor porcinecells. In coronary non-diseased arteries porcine first order coronary vasa arteriesare more first abundant order vasa than are second more order, abundant while than the reversesecond is order, seen whilein atherosclerotic the reverse ismodels. seen in Th atherosclerotice development models. of this The neovascular development vasa ofvaso- this rumneovascular
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