Osteoarthritis (OA) is the most common form of chronic musculoskeletal disorders. A migratory stem cell population termed chondrogenic progenitor cells (CPC) with in vitro chondrogenic potential was previously isolated from OA cartilage. Since intracellular Ca²⁺ signalling is an important regulator of chondrogenesis, we aimed to provide a detailed understanding of the Ca²⁺ homeostasis of CPCs. In this work, CPCs immortalised by lentiviral administration of the human telomerase reverse transcriptase (hTERT) and grown in monolayer cultures were studied. Expressions of all three IP₃Rs were confirmed, but no RyR subtypes were detected. Ca²⁺ oscillations observed in CPCs were predominantly dependent on Ca²⁺ release and store replenishment via store-operated Ca²⁺ entry; CPCs express both STIM1 and Orai1 proteins. Expressions of adenosine receptor mRNAs were verified, and adenosine elicited Ca²⁺ transients. Various P2 receptor subtypes were identified; P2Y₁ can bind ADP; P2Y₄ is targeted by UTP; and ATP may evoke Ca²⁺ transients via detected P2X subtypes, as well as P2Y₁ and P2Y₂. Enzymatic breakdown of extracellular nucleotides by apyrase completely abrogated Ca²⁺ oscillations, suggesting that an autocrine/paracrine purinergic mechanism may drive Ca²⁺ oscillations in these cells. As CPCs possess a broad spectrum of functional molecular elements of Ca²⁺ signalling, Ca²⁺-dependent regulatory mechanisms can be supposed to influence their differentiation potential.