The science behind our services
Mesenchymal stem cells (MSCs).
Mesenchymal stem cells (MSCs) are usually called stem cells, but much of the research literature now calls them stromal cells. This page covers the cell biology behind autologous bone marrow therapies: how MSCs are defined, why cell size affects where infused cells end up, how the immune system reacts to donor cells, the tiny particles cells release, how cells age, and the blood-brain barrier.
01 · Definition
MSC Classification
The International Society for Cellular Therapy (ISCT) Mesenchymal and Tissue Stem Cell Committee set three minimal criteria for mesenchymal stromal cells in 2006. A cell population must meet all three to be classified as MSCs:
- Plastic adherence. The cells must adhere to plastic under standard culture conditions.
- Tri-lineage differentiation. When stimulated in the laboratory, the cells must be able to differentiate into bone (osteoblasts), fat (adipocytes), and cartilage (chondroblasts).
- Surface-marker expression. The cells must express a specific surface-marker phenotype, positive for CD105, CD73, and CD90; negative for CD45, CD34, CD14, CD19, and HLA-DR (detailed below).
MSCs are further classified by cell source, bone marrow–derived (BM-MSCs), adipose-derived (AD-MSCs), and umbilical cord MSCs (UC-MSCs). Regardless of source, CD105, CD73, and CD90 are expressed on virtually all mesenchymal stem cells. MSCs are multipotent spindle-shaped cells with self-renewal capacities that can differentiate into related cell types in vitro or by transplantation.1
More recently, it has been found that MSCs play a more significant role in producing regenerative and immunomodulatory elements under normal conditions, as opposed to differentiation in vivo.2
In plain language
MSCs seem to work mainly through the chemical signals they release, which can adjust immune activity and support the body's own repair. Studies have not shown them turning into new cartilage, nerve, or heart cells in the body.
Figure 1 · Spindle shaped, plastic-adherent MSCs in a cultured laboratory environment.
02 · Cell size
The first-pass effect.
An often-overlooked issue in clinical intravenous human MSC (hMSC) treatments revolves around the diameter and volume of the cells being infused. The first-pass effect is a known phenomenon in the lungs3,4, mechanical trapping of infused cells in the pulmonary capillaries.
The first-pass effect occurs if the infused MSCs are larger in diameter than the pulmonary capillaries. Ex-vivo culture and expansion of BM-hMSCs leads to increases in cell diameters and volumes, surpassing the pulmonary capillaries' diameters. Bhat et al.5 reported that the average diameter of low-serum cultured BM-hMSCs is between 16.02 (±0.16) and 19.2 (±0.22) µm.
Evidence suggests that in humans, the entrapped cells in the lungs are subsequently cleared and have been found to accumulate in the spleen and liver over the ensuing hours to days after infusion.6 Most infused cells do not survive long. Research suggests the recipient's own immune cells trigger the infused MSCs to die off, and that this die-off may be part of how the cells adjust immune activity.7
Endogenous MSCs in the bone marrow are approximately 10 µm in size, enabling an enhanced ability to navigate and pass through capillaries, particularly the lungs. In contrast, undifferentiated adipose-derived stem cells (AD-SCs) are larger (mean diameter ~14.9 µm), which effectively puts AD-SCs at the upper limit of the pulmonary capillary bed diameter.
| Culture state | Mean diameter | Relative to pulmonary capillary (10–15 µm) |
|---|---|---|
| Endogenous BM-MSC (reference) | ~10 µm | Below, navigates capillary bed |
| Undifferentiated AD-MSC | ~14.9 µm | At upper end of capillary bed |
| Differentiated / activated AD-MSC | ↑ with culture days | Above, first-pass trapping likely |
| Low-serum cultured BM-hMSC (Bhat 2021) | 16.0–19.2 µm | Above, first-pass trapping likely |
Clinical implication
Cell size helps explain why cells given by IV can get caught in the lungs. Smaller cells, like the MSCs found naturally in bone marrow, are less likely to be trapped than larger lab-grown cells.
03 · Immunogenicity
Allogeneic vs autologous, revisiting "immune-privileged."
In the past, allogeneic MSCs were thought to be immune-privileged due to their lack of major histocompatibility complex (MHC) class II molecules. Results from more recent studies have shown that in vivo administration of allogeneic MSCs may provoke a strong immune response in the host.9
Your immune system spots foreign cells by proteins on their surface called MHC markers. MSCs grown in a lab carry few of these markers, which is why donor MSCs were once thought to slip past the immune system. That changes when the cells start to mature into other cell types, or when they meet interferon-gamma, a signal released during inflammation. They then make more MHC markers, and the recipient's immune system can react to donor cells. Your own cells carry your own markers, so this reaction does not apply to them.9
Joswig et al.10 evaluated the response to repeated intra-articular injections of autologous versus allogeneic BM-MSCs in an equine model. Following the second dose, the allogeneic BM-MSC recipients had elevated total nucleated cell counts in the injected joints, while no adverse immunogenic responses were seen in the autologous group. This should prompt further consideration about how to best proceed in patients requiring multiple administrations of allogeneic stem cell–based therapies.
04 · Signaling cargo
Extracellular vesicles & exosomes.
All living cells release extracellular vesicles (EVs) derived from bilayer lipid membranes. EVs transport many cell-derived molecules, nucleic acids, proteins, lipids, and metabolites, that reflect the originating cell's characteristics. Subtypes include exosomes, ectosomes, oncosomes, microvesicles, and apoptotic bodies. L. Ramos et al.11 characterized EVs released from BM-hMSCs as positive for markers CD44, CD73, and CD90.
Exosomes are mediators of intercellular communication by microRNA, the smallest EVs, with a diameter range of 30–150 nm.12 Exosomes are formed by exocytosis of multivesicular bodies (MVBs), which frees intraluminal vesicles by fusing with the plasma membrane.13 The exosomal membrane is characterized by sphingomyelin, cholesterol, ceramide, and phosphatidylserine.
Recent research has revealed that exosomes may transfer bioactive molecules, pointing to a prominent role in the pathologies of Parkinson's,14 Alzheimer's,15 spongiform encephalopathies,16 and ALS.17 This same bioactive-transport capacity may also be therapeutic: In a mouse study, MSC-derived exosomes given through the nose gathered in damaged areas of the brain.18
Why this matters clinically
Exosomes are far smaller than cells (as small as about 30 nanometers), so in principle they can reach places whole cells cannot. That is why researchers are studying them as a way to carry signals between cells. No exosome product is FDA-approved to treat any condition.
05 · Senescence
Age, disease & culture-related stem cell impairment.
Throughout an individual's lifespan, stem cells maintain a continued presence in the body, making them prone to cell damage, loss of regenerative function, senescence (inability to proliferate), and cell death.19 The buildup of toxic metabolites is theorized to be central to accumulative DNA and macromolecule damage.20 Aging is also implicated in alterations in protein homeostasis21 and mitochondrial DNA mutations22 that deplete the stem-cell pool.
Aging-related decline affects MSCs, hematopoietic stem cells (HSCs), neural stem cells (NSCs), skeletal muscle progenitor cells (SMPCs), skin stem cells (SSCs), and germ-line stem cells.23 Specific to MSCs, age-dependent bone marrow declines have been found alongside functional alterations: impairments in migratory capacity and senescence tendencies.24
Age-related stem cell impairment parallels what is found with chronic diseases:
- Diabetes
- Obesity
- Dyslipidemia
- Glucocorticoid excess
- Rheumatoid arthritis (RA)
- Systemic lupus erythematosus (SLE)
- Cardiovascular disease (CVD)
- Osteoporosis
Specific stem-cell lines impacted by each are detailed in Table 2 of Pérez, de Lucas, and Gálvez.25
Hayflick limit and culture-induced aging.
To augment clinical utility, MSCs are frequently expanded in vitro to achieve appropriate cell numbers. Population doublings (PDs) serve as a quantitative reference for culture expansion. Despite the source, MSCs demonstrate replicative senescence in vitro after repeated PDs, the Hayflick limit.26 The estimated maximum possible PDs before replicative cessation is 30–40, and even minimal passaging induces rapid MSC aging through telomere shortening.27
Expansion-induced aging raises the question of whether therapeutic emphasis should be placed on quantity or quality of MSCs employed in treatments. In a meta-analysis by Muthu et al.28 of 17 RCTs studying autologous MSC treatment in knee OA (767 patients, both cultured and uncultured):
| Outcome measure | Time point | Cultured expanded (CE) | Uncultured (UC) |
|---|---|---|---|
| VAS | 6 months | Significant | Not significant |
| VAS | 12 months | Not significant | Significant |
| WOMAC | 12 months | Not significant | Significant |
| KOOS | 12 months | Not significant | Significant |
VAS is a pain score. WOMAC and KOOS are knee symptom and function scores.
Takeaway
In this meta-analysis, uncultured cells showed a statistically significant improvement over controls at 12 months on pain (VAS) and on knee symptom and function scores (WOMAC and KOOS), and culture-expanded cells did not. Each type was compared with controls, which on its own does not show that one type beats the other, and the pooled studies differed widely.
Heterogeneity, CFUs & senescence markers.
MSC heterogeneity encompasses proliferation rate, immunophenotype, morphology, multilineage differential potential, and senescence.29 The number of colony-forming units (CFUs) consistently decreases with culture expansion, and CFU numbers become negligible after 20 passages.29
Morphologically, large MSCs in culture with increased granularity coincide with senescence.30 MSC autofluorescence has been put forth as a real-time, non-invasive, and quantifiable senescence marker.31 Other markers include β-galactosidase32 and senescence-associated α-L-fucosidase. Since telomere length decreases with each cell division until a critical-length senescence stage, telomeres predict senescence and estimate division history.33
Researchers are now testing ways to slow or reverse this aging in the lab, including MSCs made from induced pluripotent stem cells (iMSCs), gene editing, and drugs such as rapamycin.
06 · CNS access
The blood–brain barrier.
The blood–brain barrier (BBB) is the network of endothelial cells forming the central nervous system's highly selective barrier. It generally facilitates molecular transport into the brain by lipid-solubility diffusion and catalyzed transport. The BBB plays an essential role in normal brain function by maintaining homeostasis and immune-cell transport, and protects the CNS from toxins, pathogens, injury, inflammation, and disease.34 Any compromise in BBB selectiveness may allow pathogens into the CNS and cause neuroinflammation, contributing to neurodegenerative-disease progression.35
By default, a limited number of solutes can passively cross the BBB without active transport, gases (O₂, CO₂), low-molecular-weight lipid-soluble molecules under 400 Da, or molecules with fewer than eight hydrogen bonds.36
The degree to which the BBB represents an active barrier to MSCs entering the CNS has not been fully elucidated. A 2011 lab study found that MSCs can pass through a layer of brain blood-vessel cells grown in a dish.37 Whether this happens in people, and whether it helps, is not yet known.
MSC homing may occur as a systemic or nonsystemic process. Nonsystemic homing represents direct inoculation into targeted tissues, where local cytokines guide cells to injured areas. Systemic homing refers to administration away from injured tissues.38 Several models describe the mechanism, MSCs leaving the circulation by endothelial integration, migration through the endothelial barrier, basement-membrane penetration, and formation of plasmic podia to infiltrate target tissues.39
Why this informs our clinical framing
Intranasal delivery, via olfactory and trigeminal pathways, is being investigated specifically because it bypasses systemic circulation and the BBB as a gating constraint.
References
Selected citations.
Sources cited in this article, numbered as they appear in the text.
- Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–7.
- Guimarães-Camboa N, Cattaneo P, Sun Y, et al. Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell. 2017;20(3):345–359.e5.
- Toma C, Wagner WR, Bowry S, et al. Fate of culture-expanded mesenchymal stem cells in the microvasculature: in vivo observations of cell kinetics. Circ Res. 2009;104(3):398–402.
- Fischer UM, Harting MT, Jimenez F, et al. Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect. Stem Cells Dev. 2009;18(5):683–692.
- Bhat S, Viswanathan P, Chandanala S, et al. Expansion and characterization of bone marrow derived human mesenchymal stromal cells in serum-free conditions. Sci Rep. 2021;11(1):3403.
- Krueger TEG, Thorek DLJ, Denmeade SR, et al. Concise review: mesenchymal stem cell-based drug delivery: the good, the bad, the ugly, and the promise. Stem Cells Transl Med. 2018;7(9):651–663.
- Galleu A, Riffo-Vasquez Y, Trento C, et al. Apoptosis in mesenchymal stromal cells induces in vivo recipient-mediated immunomodulation. Sci Transl Med. 2017;9(416):eaam7828.
- MilliporeSigma. Rapid analysis of human adipose-derived stem cells and 3T3-L1 differentiation towards adipocytes using the Scepter 2.0 cell counter. Application note.
- Ankrum JA, Ong JF, Karp JM. Mesenchymal stem cells: immune evasive, not immune privileged. Nat Biotechnol. 2014;32(3):252–60.
- Joswig AJ, Mitchell A, Cummings KJ, et al. Repeated intra-articular injection of allogeneic mesenchymal stem cells causes an adverse response compared to autologous cells in the equine model. Stem Cell Res Ther. 2017;8(1):42.
- L Ramos T, Sánchez-Abarca LI, Muntión S, et al. MSC surface markers (CD44, CD73, and CD90) can identify human MSC-derived extracellular vesicles by conventional flow cytometry. Cell Commun Signal. 2016;14:2.
- Sidhom K, Obi PO, Saleem A. A review of exosomal isolation methods: is size exclusion chromatography the best option? Int J Mol Sci. 2020;21(18):6466.
- Kowal J, Tkach M, Théry C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol. 2014;29:116–125.
- Emmanouilidou E, Melachroinou K, Roumeliotis T, et al. Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J Neurosci. 2010;30(20):6838–6851.
- Rajendran L, Honsho M, Zahn TR, et al. Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc Natl Acad Sci U S A. 2006;103(30):11172–11177.
- Fevrier B, Vilette D, Archer F, et al. Cells release prions in association with exosomes. Proc Natl Acad Sci U S A. 2004;101(26):9683–9688.
- Gomes C, Keller S, Altevogt P, et al. Evidence for secretion of Cu,Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis. Neurosci Lett. 2007;428(1):43–46.
- Perets N, Betzer O, Shapira R, et al. Golden exosomes selectively target brain pathologies in neurodegenerative and neurodevelopmental disorders. Nano Lett. 2019;19(6):3422–3431.
- Yun MH. Changes in regenerative capacity through lifespan. Int J Mol Sci. 2015;16(10):25392–25432.
- Yang SR, Park JR, Kang KS. Reactive oxygen species in mesenchymal stem cell aging: implication to lung diseases. Oxid Med Cell Longev. 2015;2015:486263.
- Tomaru U, Takahashi S, Ishizu A, et al. Decreased proteasomal activity causes age-related phenotypes and promotes the development of metabolic abnormalities. Am J Pathol. 2012;180(3):963–972.
- Bratic A, Larsson NG. The role of mitochondria in aging. J Clin Invest. 2013;123(3):951–957.
- Schultz MB, Sinclair DA. When stem cells grow old: phenotypes and mechanisms of stem cell aging. Development. 2016;143(1):3–14.
- Kasper G, Mao L, Geissler S, et al. Insights into mesenchymal stem cell aging: involvement of antioxidant defense and actin cytoskeleton. Stem Cells. 2009;27(6):1288–1297.
- Pérez LM, de Lucas B, Gálvez BG. Unhealthy stem cells: when health conditions upset stem cell properties. Cell Physiol Biochem. 2018;46(5):1999–2016.
- Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res. 1961;25:585–621.
- Baxter MA, Wynn RF, Jowitt SN, et al. Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells. 2004;22(5):675–682.
- Muthu S, Kartheek RR, Jeyaraman N, et al. Is culture expansion necessary in autologous mesenchymal stromal cell therapy to obtain superior results in the management of knee osteoarthritis? Meta-analysis of randomized controlled trials. Bioengineering (Basel). 2021;8(12):220.
- Schellenberg A, Stiehl T, Horn P, et al. Population dynamics of mesenchymal stromal cells during culture expansion. Cytotherapy. 2012;14(4):401–411.
- Block TJ, Marinkovic M, Tran ON, et al. Restoring the quantity and quality of elderly human mesenchymal stem cells for autologous cell-based therapies. Stem Cell Res Ther. 2017;8(1):239.
- Bertolo A, Baur M, Guerrero J, et al. Autofluorescence is a reliable in vitro marker of cellular senescence in human mesenchymal stromal cells. Sci Rep. 2019;9(1):2074.
- Dimri GP, Lee X, Basile G, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A. 1995;92(20):9363–9367.
- Montpetit AJ, Alhareeri AA, Montpetit M, et al. Telomere length: a review of methods for measurement. Nurs Res. 2014;63(4):289–299.
- Daneman R, Prat A. The blood–brain barrier. Cold Spring Harb Perspect Biol. 2015;7(1):a020412.
- Graham NSN, Sharp DJ. Understanding neurodegeneration after traumatic brain injury: from mechanisms to clinical trials in dementia. J Neurol Neurosurg Psychiatry. 2019;90(11):1221–1233.
- Pardridge WM. Drug transport across the blood–brain barrier. J Cereb Blood Flow Metab. 2012;32(11):1959–1972.
- Matsushita T, Kibayashi T, Katayama T, et al. Mesenchymal stem cells transmigrate across brain microvascular endothelial cell monolayers through transiently formed inter-endothelial gaps. Neurosci Lett. 2011;502(1):41–45.
- Chia YC, Anjum CE, Yee HR, et al. Stem cell therapy for neurodegenerative diseases: how do stem cells bypass the blood-brain barrier and home to the brain? Stem Cells Int. 2020;2020:8889061.
- Steingen C, Brenig F, Baumgartner L, et al. Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells. J Mol Cell Cardiol. 2008;44(6):1072–1084.
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